%0 Journal Article
%J Nature
%D In Press
%T Hybrid speciation driven by multilocus introgression of ecological traits
%A Rosser, Neil *
%A Seixas, Fernando *
%A Queste, Lucie M.
%A Cama, Bruna
%A Mori-Pezo, Ronald
%A Kryvokhyzha, Dmytro
%A Nelson, Michaela
%A Eleres de Figueiredo, Clarisse Mendes
%A Freitas, André Victor Lucci
%A Joron, Mathieu
%A Kozak, Krzysztof
%A Lamas, Gerardo
%A Martins, Ananda R.P.
%A McMillan, W. Owen
%A Ready, Jonathan
%A Rueda-Muñoz, Nicol
%A Salazar, Camilo
%A Salazar, Patricio
%A Schulz, Stefan
%A Shirai, Leila T.
%A Silva-Brandão, Karina L.
%A Mallet, James
%A Dasmahapatra, Kanchon K.
%X Hybridisation allows adaptations to be shared among lineages and may trigger the evolution of new species. However, convincing examples of homoploid hybrid speciation remain rare because it is challenging to demonstrate that hybridisation was critical in generating reproductive isolation. Here we combine population genomic analysis with quantitative trait locus mapping of species-specific traits to dissect a new case of hybrid speciation in Heliconius butterflies. We show that H. elevatus is a hybrid species that is sympatric with both parents and has persisted as an independently evolving lineage for at least 180,000 years. This is despite pervasive and ongoing gene flow with one parent, H. pardalinus, which homogenises 99% of their genomes. The remaining 1% introgressed from the other parent, H. melpomene, and is scattered widely across the H. elevatus genome in islands of divergence from H. pardalinus. These islands harbour multiple traits under disruptive selection, including colour pattern, wing shape, hostplant preference, sex pheromones and mate choice. Collectively, these traits place H. elevatus on its own adaptive peak and permit coexistence with both parents. Our results show that speciation was driven by introgression of ecological traits and that speciation with gene flow is possible with a multilocus genetic architecture.
%B Nature
%V xxx
%P 000
%8 2024
%G eng
%0 Journal Article
%J Cold Spring Harbor Perspectives in Biology
%D 2024
%T The Role of Hybridization in Species Formation and Persistence
%A Peñalba, Joshua V.
%A Runemark, Anna
%A Meier, Joana I.
%A Singh, Pooja
%A Wogan, Guinevere O.U.
%A Sánchez-Guillén, Rosa
%A Mallet, James
%A Rometsch, Sina J.
%A Menon, Mitra
%A Seehausen, Ole
%A Kulmuni, Jonna
%A Pereira, Ricardo J.
%X Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown of reproductive isolation and even to the reversal of speciation. However, modern genomic and analytical methods have shown that hybridization is common in some of the most diverse clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to introgression of adaptive alleles, to the formation of hybrid species, and even to entire species radiations. In this review, we identify consensus among diverse research programs to show how the field has progressed. Hybridization is a multifaceted evolutionary process that can strongly influence species formation and facilitate adaptation and persistence of species in a rapidly changing world. Progress on testing this hypothesis will require cooperation among different subdisciplines.
%B Cold Spring Harbor Perspectives in Biology
%P a041445
%8 2024/03/04
%G eng
%U http://cshperspectives.cshlp.org/content/early/2024/03/01/cshperspect.a041445.abstractN2 - Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes
%! Cold Spring Harbor Perspectives in Biology
%0 Journal Article
%J Proceedings of the National Academy of Sciences, USA
%D 2024
%T Pervasive mimicry in flight behavior among aposematic butterflies
%A Page, Edward
%A Queste, Lucie M.
%A Rosser, Neil
%A Salazar, Patricio A.
%A Nadeau, Nicola J.
%A Mallet, James
%A Srygley, Robert B.
%A McMillan, W. Owen
%A Dasmahapatra, Kanchon K.
%X Flight was a key innovation in the adaptive radiation of insects. However, it is a complex trait influenced by a large number of interacting biotic and abiotic factors, making it difficult to unravel the evolutionary drivers. We investigate flight patterns in neotropical heliconiine butterflies, well known for mimicry of their aposematic wing color patterns. We quantify the flight patterns (wing beat frequency and wing angles) of 351 individuals representing 29 heliconiine and 9 ithomiine species belonging to ten color pattern mimicry groupings. For wing beat frequency and up wing angles, we show that heliconiine species group by color pattern mimicry affiliation. Convergence of down wing angles to mimicry groupings is less pronounced, indicating that distinct components of flight are under different selection pressures and constraints. The flight characteristics of the Tiger mimicry group are particularly divergent due to convergence with distantly related ithomiine species. Predator-driven selection for mimicry also explained variation in flight among subspecies, indicating that this convergence can occur over relatively short evolutionary timescales. Our results suggest that the flight convergence is driven by aposematic signaling rather than shared habitat between comimics. We demonstrate that behavioral mimicry can occur between lineages that have separated over evolutionary timescales ranging from <0.5 to 70 My.
%B Proceedings of the National Academy of Sciences, USA
%V 121
%P e2300886121
%G eng
%U https://doi.org/10.1073/pnas.2300886121
%N 11
%0 Web Page
%D 2024
%T Colour patterns in Lepidoptera evolved mainly as signals to predators. Heliconius are indeed Müllerian mimics. Reply to Mouy (2022).
%A Mallet, James
%X A recent paper in the journal Evolutionary Ecology by Henri Mouy, an independent researcher and theoretician who gives his address as “City of Westminster, London, UK,” argues that aposematism (warning colour) and Müllerian mimicry are problematic hypotheses. Instead, he claims that the bright colours and apparent colour pattern mimicry act primarily as an intraspecific or interspecific communication device to enable aggregation. In this critique, I show that the long-standing understanding that aposematic and mimetic colour patterns communicate directly with predators is much more likely than Mouy’s aggregation hypothesis.
%B heliconius.org
%G eng
%U https://www.heliconius.org/2024/no-evidence-for-henri-mouys-views-aposematism-and-mimicry/
%0 Journal Article
%J Molecular Biology and Evolution
%D 2023
%T Inferring the direction of introgression using genomic sequence data
%A Thawornwattana, Yuttapong
%A Huang, Jun
%A Flouri, Tomáš
%A Mallet, James
%A Yang, Ziheng
%X Genomic data are informative about the history of species divergence and interspecific gene flow, including the direction, timing, and strength of gene flow. However, gene flow in opposite directions generates similar patterns in multilocus sequence data, such as reduced sequence divergence between the hybridizing species. As a result, inference of the direction of gene flow is challenging. Here we investigate the information about the direction of gene flow present in genomic sequence data using likelihood-based methods under the multispecies-coalescentwith-introgression model. We analyze the case of two species, and use simulation to examine cases with three or four species. We find that it is easier to infer gene flow from a small population to a large one than in the opposite direction, and easier to infer inflow (gene flow from outgroup species to an ingroup species) than outflow (gene flow from an ingroup species to an outgroup species). It is also easier to infer gene flow if there is a longer time of separate evolution between the initial divergence and subsequent introgression. When introgression is assumed to occur in the wrong direction, the time of introgression tends to be correctly estimated and the Bayesian test of gene flow is often significant, while estimates of introgression probability can be even greater than the true probability. We analyze genomic sequences from Heliconius butterflies to demonstrate that typical genomic datasets are informative about the direction of interspecific gene flow, as well as its timing and strength.
%B Molecular Biology and Evolution
%V 40
%P msad178
%G eng
%U https://doi.org/10.1093/molbev/msad178
%N 8
%0 Journal Article
%J eLife
%D 2023
%T Major patterns in the introgression history of Heliconius butterflies
%A Thawornwattana, Yuttapong
%A Seixas, Fernando A.
%A Yang, Ziheng
%A Mallet, James
%X Gene flow between species is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes reconstruction of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events inHeliconiusbutterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the "melpomene-silvaniform" group, which shows extensive historical and on-going gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that H. aoede most likely represents the earliest- branching lineage of the genus and that "silvaniform" species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.
%B eLife
%V 12
%P RP90656
%8 June 23, 2023.
%G eng
%U https://doi.org/10.7554/eLife.90656.3
%0 Journal Article
%J Proceedings of the National Academy of Sciences, USA
%D 2023
%T A polygenic explanation for Haldane's Rule in butterflies
%A Xiong, Tianzhu
%A Tarikere, Shreeharsha
%A Rosser, Neil
%A Li, Xueyan
%A Yago, Masaya
%A Mallet, James
%X The fitness of animal hybrids follows two empirical rules: hybrids of the heterogametic sex aremore unfit (Haldane’s Rule), and the sex chromosome is disproportionately involved in incompatibility (the large-X/Z effect). Whether these rules result from genetic mechanisms shared across taxa remains unknown, and existing explanations rarely consider female heterogametic taxa such as butterflies. Here, we investigate hybrid incompatibilities inPapilioandHeliconiusbutterflies, and show that defects coincide with unbalanced introgression between the Z chromosome and its genetic background. This polygenic mechanism predicts both rules because introgressed ancestry on the Z chromosome is more skewed in females, and is more variable than on all autosomes. Therefore, the explanation for both rules in butterflies shares little similarity with prevailing theories relying on dominance.
%B Proceedings of the National Academy of Sciences, USA
%V 120
%P e2300959120
%8 2023
%G eng
%U https://doi.org/10.1073/pnas.2300959120
%N 44
%0 Journal Article
%J Molecular Biology and Evolution
%D 2022
%T Inference of gene flow between species under misspecified models
%A Huang, Jun
%A Thawornwattana, Yuttapong
%A Flouri, Tomáš
%A Mallet, James
%A Yang, Ziheng
%X Genomic sequence data provide a rich source of information about the history of species divergence and interspecific hybridization or introgression. Despite recent advances in genomics and statistical methods, it remains challenging to infer gene flow, and as a result, one may have to estimate introgression rates and times under misspecified models. Here we use mathematical analysis and computer simulation to examine estimation bias and issues of interpretation when the model of gene flow is misspecified in analysis of genomic datasets, for example, if introgression is assigned to the wrong lineages. In the case of two species, we establish a correspondence between the migration rate in the continuous migration model and the introgression probability in the introgression model. When gene flow occurs continuously through time but in the analysis is assumed to occur at a fixed time point, common evolutionary parameters such as species divergence times are surprisingly well estimated. However, the time of introgression tends to be estimated towards the recent end of the period of continuous gene flow. When introgression events are assigned incorrectly to the parental or daughter lineages, introgression times tend to collapse onto species divergence times, with introgression probabilities underestimated. Overall, our analyses suggest that the simple introgression model is useful for extracting information concerning between-specific gene flow and divergence even when the model may be misspecified. However, for reliable inference of gene flow it is important to include multiple samples per species, in particular, from hybridizing species.
%B Molecular Biology and Evolution
%V 39
%P 1-19
%G eng
%U https://doi.org/10.1093/molbev/msac237
%N 12
%0 Journal Article
%J Evolution
%D 2022
%T On the impermanence of species: the collapse of genetic incompatibilities in hybridizing populations
%A Xiong, Tianzhu
%A Mallet, James
%X Species pairs often become genetically incompatible during divergence, which is an important source of reproductive isolation. An idealized picture is often painted where incompatibility alleles accumulate and fix between diverging species. However, recent studies have shown both that incompatibilities can collapse with ongoing hybridization, and that incompatibility loci can be polymorphic within species. This paper suggests some general rules for the behavior of incompatibilities under hybridization. In particular, we argue that redundancy of genetic pathways can strongly affect the dynamics of intrinsic incompatibilities. Since fitness in genetically redundant systems is unaffected by introducing a few foreign alleles, higher redundancy decreases the stability of incompatibilities during hybridization, but also increases tolerance of incompatibility polymorphism within species. We use simulations and theories to show that this principle leads to two types of collapse: in redundant systems, exemplified by classical Dobzhansky–Muller incompatibilities, collapse is continuous and approaches a quasi-neutral polymorphism between broadly sympatric species, often as a result of isolation-by-distance. In nonredundant systems, exemplified by co-evolution among genetic elements, incompatibilities are often stable, but can collapse abruptly with spatial traveling waves. As both types are common, the proposed principle may be useful in understanding the abundance of genetic incompatibilities in natural populations.
%B Evolution
%V 76
%P 2498-2512
%G eng
%U https://doi.org/10.1111/evo.14626
%N 11
%0 Journal Article
%J Journal of Evolutionary Biology
%D 2022
%T Reproductive isolation is a heuristic, not a measure: a commentary on Westram et al., 2022
%A Mallet, James
%A Mullen, Sean P.
%X Reproductive isolation is the heuristic basis of the biological species concept, but what is it? Westram et al. (this issue) propose that it is a measurable quantity, "barrier strength," that prevents gene flow among populations. However, their attempt to make the concept of reproductive isolation more scientific is unlikely to satisfy the diverse opinions of all evolutionary biologists. There are many different opinions about the nature of species, even under the biological species concept. Complete reproductive isolation, where gene flow is effectively zero, is regarded by some biologists as an important end point of speciation. Others, including Westram et al., argue for a more nuanced approach, and they also suggest that reproductive isolation may differ in different parts of the genome due to variation in genetic linkage to divergently selected loci. In contrast to both these approaches, we favour as a key criterion of speciation the stable coexistence of divergent populations in sympatry. Obviously, such populations must be reproductively isolated in some sense, but neither the fraction of the genome that is exchanged, nor measures of overall barrier strength acting on neutral variation will yield very precise predictions as to species status. Although an overall measure of reproductive isolation is virtually unattainable for these reasons, its early generation components, such as assortative mating, divergent selection, or hybrid inviability and sterility are readily measurable and remain informative. For example, we can make the prediction that to remain divergent in sympatry, almost all sexual species will require strong assortative mating, as well as some sort of ecological or intrinsic selection against hybrids and introgressed variants.
%B Journal of Evolutionary Biology
%V 35
%P 1175-1182
%G eng
%U https://doi.org/10.1111/jeb.14052
%N 9
%0 Journal Article
%J Molecular Ecology
%D 2022
%T Sympatric speciation by allochrony?
%A Rosser, Neil
%A Seixas, Fernando
%A Mallet, James
%X Sympatric speciation was once thought most improbable, but careful study of some systems, particularly the apple maggot (Rhagoletis pomonella) and related Rhagoletis species, has led to its reinstatement as a likely mode of speciation in some cases. Different species and host races in this clade of flies often have highly specialized host preference, and along with frequent evolutionary shifts to different fruit species between sister taxa, there is a likely effect of the timing of adult emergence that follows host fruiting phenology. This is known as "allochronic" isolation (from the Greek, meaning "different timing"). This overview covers recent discoveries by Inskeep et al. (Molecular Ecology, 2021) showing how allochrony is a major factor in preventing gene flow between a pair of sister species of Rhagoletis on different host fruits. Although the authors do not claim to prove sympatric speciation, it does seem very likely, and the work clearly underscores how readily host shifts via allochrony can aid sympatric speciation.
%B Molecular Ecology
%V 31
%P 3975-3978
%G eng
%U https://doi.org/10.1111/mec.16599
%0 Journal Article
%J Evolution
%D 2022
%T The making of a moth man (book review of: Grant, Bruce S. 2021. Observing Evolution)
%A Mallet, James
%B Evolution
%V 76
%P 1362-1365
%G eng
%U https://academic.oup.com/evolut/article/76/6/1362/6728740
%N 6
%0 Journal Article
%J eLife
%D 2022
%T Admixture of evolutionary rates across a butterfly hybrid zone
%A Xiong, Tianzhu
%A Li, Xueyan
%A Yago, Masaya
%A Mallet, James
%X Hybridization is a major evolutionary force that can erode genetic differentiation between species, whereas reproductive isolation maintains such differentiation. In studying a hybrid zone between the swallowtail butterflies Papilio syfanius and Papilio maackii (Lepidoptera: Papilionidae), we made the unexpected discovery that genomic substitution rates are unequal between the parental species. This phenomenon creates a novel process in hybridization, where genomic regions most affected by gene flow evolve at similar rates between species, while genomic regions with strong reproductive isolation evolve at species-specific rates. Thus, hybridization mixes evolutionary rates in a way similar to its effect on genetic ancestry. Using coalescent theory, we show that the rate-mixing process provides distinct information about levels of gene flow across different parts of genomes, and the degree of rate-mixing can be predicted quantitatively from relative sequence divergence (FSTFST) between the hybridizing species at equilibrium. Overall, we demonstrate that reproductive isolation maintains not only genomic differentiation, but also the rate at which differentiation accumulates. Thus, asymmetric rates of evolution provide an additional signature of loci involved in reproductive isolation
%B eLife
%V 11
%P e78135
%G eng
%U https://doi.org/10.7554/eLife.78135
%0 Book Section
%B Encyclopedia of Biodiversity
%D 2022
%T Species, concepts of
%A Mallet, James
%A Seixas, Fernando
%A Thawornwattana, Yuttapong
%X What are species? We take a historical approach to demonstrate how our understanding of the nature of species has changed since Darwin's time until the current postgenomic era. If species are fundamental units of nature (like cells, or organisms, say), as some scientists believe, then their underlying basis has yet to be revealed. Instead, it seems more likely that the species rank in taxonomy is a man-made distinction; a heuristic cut-off that can perhaps be agreed upon bybiologists to enable communication on issues of biodiversity, human health, agriculture, and conservation.
%B Encyclopedia of Biodiversity
%I Elsevier
%G eng
%0 Journal Article
%J Molecular Ecology
%D 2022
%T Complex basis of hybrid female sterility and Haldane’s rule in Heliconius butterflies: Z-linkage and epistasis
%A Rosser, Neil
%A Nathaniel B. Edelman
%A Queste, Lucie M.
%A Nelson, Michaela
%A Seixas, Fernando
%A Dasmahapatra, Kanchon K.
%A Mallet, James
%X Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex – a pattern known as Haldane’s rule. The genetics of Haldane’s Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the “large X effect” in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane’s Rule.
%B Molecular Ecology
%V 31
%P 959-977
%G eng
%U https://doi.org/10.1111/mec.16272
%0 Journal Article
%J Systematic Biology
%D 2022
%T Full-likelihood genomic analysis clarifies a complex history of species divergence and introgression: the example of the erato-sara group of Heliconius butterflies
%A Thawornwattana, Yuttapong
%A Seixas, Fernando A.
%A Yang, Ziheng
%A Mallet, James
%X Introgression plays a key role in adaptive evolution and species diversification in many groups of species including Heliconius butterflies. However, frequent hybridization and gene flow between species makes estimation of the species phylogeny challenging, especially for rapidly speciating species within adaptive radiations. Here, we analyze the genomic sequences from six members of the erato-sara clade of Heliconius butterflies to infer the species phylogeny and cross-species introgression events. To avoid heterozygote phasing errors in haploid sequences commonly produced by genome assembly methods, we processed and compiled unphased diploid sequence alignments, with the analytical methods averaging over uncertainties in heterozygote phase resolution. We use likelihood-based methods under the multispecies coalescent (MSC) model with and without gene flow to accommodate random fluctuations in genealogical history across the genome due to deep coalescence. There is robust evidence of introgression across the genome, both among distantly related species deep in the phylogeny and between sister species in shallow parts of the tree. We obtain estimates of population parameters such as introgression times and probabilities, species divergence times, and population sizes for modern and ancestral species. We confirm ancestral gene flow between the sara clade and an ancestral population of likely hybrid origin of H. telesiphe, a likely hybrid origin of H. hecalesia, and gene flow between the sister species H. erato and H. himera. Our approach also demonstrates how introgression among ancestral species can explain the history of two chromosomal inversions deep in the phylogeny of the group. For the first time, we not only test for the presence of cross-species gene flow, but also estimate its direction, timing and magnitude, extracting rich historical information of species divergence and gene flow from genomic data
%B Systematic Biology
%V 71
%P 1159-1177
%8 2021
%G eng
%U https://doi.org/10.1093/sysbio/syac009
%N 5
%0 Journal Article
%J Diversity and Distributions
%D 2021
%T Anthropogenic pressures coincide with Neotropical biodiversity hotspots in a flagship butterfly group
%A Doré, Maël
%A Willmott, Keith
%A Leroy,Nicolas
%A Chazot, Nicolas
%A Mallet, James
%A Freitas, André V.L.
%A Hall, Jason P. W.
%A Lamas, Gerardo
%A Dasmahapatra, Kanchon K.
%A Fontaine, Colin
%A Elias, Marianne
%B Diversity and Distributions
%V 28
%P 2912-2930
%G eng
%U https://doi.org/10.1111/ddi.13455
%0 Book Section
%B Encyclopedia of Biodiversity
%D 2021
%T Subspecies, Semispecies, Superspecies
%A Mallet, James
%B Encyclopedia of Biodiversity
%I Elsevier
%G eng
%0 Journal Article
%J Annual Review of Genetics
%D 2021
%T Prevalence and adaptive impact of introgression
%A Nathaniel B. Edelman
%A Mallet, James
%X Alleles that introgress between species can influence the evolutionary and ecological fate of species exposed to novel environments. Hybrid offspring of different species are often unfit, and yet it has long been argued that introgression can be a potent force in evolution, especially in plants. Over the last two decades, genomic data have increasingly provided evidence that introgression is a critically important source of genetic variation and that this additional variation can be useful in adaptive evolution of both animals and plants. Here, we review factors that influence the probability that foreign genetic variants provide long-term benefits (so-called adaptive introgression) and discuss their potential benefits. We find that introgression plays an important role in adaptive evolution, particularly when a species is far from its fitness optimum, such as when they expand their range or are subject to changing environments.
%B Annual Review of Genetics
%V 55
%P 265-283
%8 2021
%G eng
%U http://www.annualreviews.org/eprint/VISBKA6WASPVFEAIN7SH/full/10.1146/annurev-genet-021821-020805
%0 Journal Article
%J Genome Biology and Evolution
%D 2021
%T Synteny-based genome assembly for 16 species of Heliconius butterflies, and an assessment of structural variation across the genus
%A Seixas, Fernando A.
%A Nathaniel B. Edelman
%A Mallet, James
%X Heliconius butterflies (Lepidoptera: Nymphalidae) are a group of 48 neotropical species widely studied in evolutionary research. Despite the wealth of genomic data generated in past years, chromosomal level genome assemblies currently exist for only two species, Heliconius melpomene and H. erato, each a representative of one of the two major clades of the genus. Here, we use these reference genomes to improve the contiguity of previously published draft genome assemblies of 16 Heliconius species. Using a reference-assisted scaffolding approach, we place and order the scaffolds of these genomes onto chromosomes, resulting in 95.7-99.9% of their genomes anchored to chromosomes. Genome sizes are somewhat variable among species (270-422 Mb) and in one small group of species (H. hecale, H. elevatus and H. pardalinus) expansions in genome size are driven mainly by repetitive sequences that map to four small regions in the H. melpomene reference genome. Genes from these repeat regions show an increase in exon copy number, an absence of internal stop codons, evidence of constraint on non-synonymous changes, and increased expression, all of which suggest that at least some of the extra copies are functional. Finally, we conducted a systematic search for inversions and identified five moderately large inversions fixed between the two major Heliconius clades. We infer that one of these inversions was transferred by introgression between the lineages leading to the erato/sara and burneyi/doris clades. These reference-guided assemblies represent a major improvement in Heliconius genomic resources that enable further genetic and evolutionary discoveries in this genus.
%B Genome Biology and Evolution
%V 13
%P evab069
%8 2021
%G eng
%U https://doi.org/10.1093/gbe/evab069
%N 7
%0 Journal Article
%J Ecography
%D 2021
%T The Amazon river is a suture zone for a polyphyletic group of co-mimetic heliconiine butterflies
%A Rosser, Neil
%A Shirai, Leila T.
%A Dasmahapatra, Kanchon K.
%A Mallet, James
%A Freitas, André V.L.
%B Ecography
%V 43
%P 177-187
%G eng
%U https://onlinelibrary.wiley.com/doi/abs/10.1111/ecog.05282
%N 2
%0 Journal Article
%J National Science Review
%D 2020
%T Alternative views of biological species: reproductively isolated units or genotypic clusters?
%A Mallet, J.
%X
Wang et al. have recently outlined their thoughts on two ideas about species: the biological species concept (BSC), and the genic view of speciation. Although both are based on reproductive isolation, the genic view, they argue, is likely preferred due to the possibility of allowing considerable gene flow among species, which is arguably what recent genomic data shows. These data, however, mostly failed to distinguish between the BSC and the genic view according to Wang et al., because it could not be ruled out that the observed introgression occurred early in speciation, when both models allow gene flow. I propose that the lack of resolution in the authors' debate is chiefly due to the difficulty of deciding when speciation is "complete" under both views tested. I agree with Wang et al. that the study of reproductive isolation is worthwhile in order to understand speciation, but I prefer to use a simpler, third criterion for speciation: the acquisition of genetic differences that allow persistence of distinguishable populations in spite of geographic overlap and the potential for continued gene flow. Under this multilocus "genotypic cluster" view, gene flow may take place at any time after species are recognized, and we do not have to decide whether gene flow is early or late in the speciation process. I detail recent genomic evidence from Anopheles mosquitoes and Heliconius butterflies showing that such "leaky" species seem to be able to coexist in spite of massive levels of introgression, often among non-sister species that show hybrid sterility in one sex.
%B National Science Review
%V 8
%P 1401-1407
%8 2020
%G eng
%U https://doi.org/10.1093/nsr/nwaa116
%N 7
%0 Journal Article
%J Molecular Ecology
%D 2020
%T Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone
%A Gauthier, J.
%A de Silva, D. L.
%A Gompert, Z.
%A Whibley, A.
%A Houssin, C.
%A Le Poul, Y.
%A McClure, M.
%A Lemaitre, C.
%A Legeai, F.
%A Mallet, J.
%A Elias, M.
%B Molecular Ecology
%V 29
%P 1328-1343
%G eng
%U https://doi.org/10.1111/mec.15403
%N 7
%0 Journal Article
%J Insect Biochemistry and Molecular Biology
%D 2020
%T Excess melanin precursors rescue defective cuticular traits in stony mutant silkworms probably by upregulating four genes encoding RR1-type larval cuticular proteins
%A Qiao, Liang
%A Yan, Zheng-wen
%A Xiong, Gao
%A Hao, You-jin
%A Wang, Ri-xin
%A Hu, Hai
%A Song, Jiang-bo
%A Tong, Xiao-ling
%A Che, Lin-rong
%A He, Song-zhen
%A Chen, Bin
%A Mallet, James
%A Lu, Cheng
%A Dai, Fang-yin
%K Cuticle features
%K Cuticular protein-encoding genes
%K Induction
%K Melanic coloring
%X Melanin and cuticular proteins are vital cuticle components in insects. Cuticular defects caused by mutations in cuticular protein-encoding genes can obstruct melanin deposition. The effects of changes in melanin on the expression of cuticular protein-encoding genes, the cuticular and morphological traits, and the origins of these effects are unknown. We found that the cuticular physical characteristics and the expression patterns of larval cuticular protein-encoding genes markedly differed between the melanic and non-melanic integument regions. By using four p multiple-allele color pattern mutants with increasing degrees of melanism (+p, pM, pS, and pB), we found that the degree of melanism and the expression of four RR1-type larval cuticular protein-encoding genes (BmCPR2, BmLcp18, BmLcp22, and BmLcp30) were positively correlated. By modulating the content of melanin precursors and the expression of cuticular protein-encoding genes in cells in tissues and in vivo, we showed that this positive correlation was due to the induction of melanin precursors. More importantly, the melanism trait introduced into the BmCPR2 deletion strain Dazao-stony induced up-regulation of three other similar chitin-binding characteristic larval cuticular protein-encoding genes, thus rescuing the cuticular, morphological and adaptability defects of the Dazao-stony strain. This rescue ability increased with increasing melanism levels. This is the first study reporting the induction of cuticular protein-encoding genes by melanin and the biological importance of this induction in affecting the physiological characteristics of the cuticle.
%B Insect Biochemistry and Molecular Biology
%V 119
%P 103315
%8 2020
%@ 0965-1748
%G eng
%U http://www.sciencedirect.com/science/article/pii/S0965174820300035
%! Insect Biochemistry and Molecular Biology
%0 Journal Article
%J Journal of Heredity
%D 2020
%T Comparing adaptive radiations across space, time, and taxa
%A Gillespie, Rosemary G.
%A Bennett, Gordon M.
%A De Meester, Luc
%A Feder, Jeffrey L.
%A Fleischer, Robert C.
%A Harmon, Luke J.
%A Hendry, Andrew P.
%A Knope, Matthew L.
%A Mallet, James
%A Martin, Christopher
%A Parent, Christine E.
%A Patton, Austin H.
%A Pfennig, Karin S.
%A Rubinoff, Daniel
%A Schluter, Dolph
%A Seehausen, Ole
%A Shaw, Kerry L.
%A Stacy, Elizabeth
%A Stervander, Martin
%A James T. Stroud
%A Wagner, Catherine
%A Wogan, Guinevere Ou
%X Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life
%B Journal of Heredity
%V 111
%P 1-20
%G eng
%U https://academic.oup.com/jhered/advance-article/doi/10.1093/jhered/esz064/5709827?guestAccessKey=403e64d2-8440-4c16-bfb7-6cefb0b3d224
%N 1
%0 Web Page
%D 2019
%T “Deep learning on butterfly phenotypes tests evolution’s oldest mathematical model” [a critique]
%A Mallet, James
%X Overall, this is a fascinating and complicated paper. It achieves for the first time a machine learning classification of the mimicry patterns in Heliconius erato and H. melpomene. But I believe it does not yet prove the case for coevolution between these two iconic co-mimics.
%B heliconius.org
%G eng
%U https://www.heliconius.org/2019/deep-learning-on-butterfly-phenotypes-tests-evolutions-oldest-mathematical-model/
%0 Journal Article
%J Science
%D 2019
%T Genomic architecture and introgression shape a butterfly radiation
%A Edelman, N.B.
%A Frandsen, P.B.
%A Miyagi, M.
%A Clavijo, B.
%A Davey, J.
%A Dikow, R.B.
%A García-Accinelli, G.
%A Van Belleghem, S.M.
%A Patterson, N.
%A Neafsey, D. E.
%A Challis, R.
%A Kumar, S.
%A Moreira, G.R.P.
%A Salazar, C.
%A Chouteau, M.
%A Counterman, B. A.
%A Papa, R.
%A Blaxter, M.
%A Reed, R. D.
%A Dasmahapatra, K. K.
%A Kronforst, M.
%A Joron, M.
%A Jiggins, C. D.
%A McMillan, W. O.
%A Di Palma, F.
%A Blumberg, A.J.
%A Wakeley, J.
%A Jaffe, D.
%A Mallet, J.
%X
Following gene flow in butterfly genomes
The role of hybridization in evolution and species radiations has long been debated. In Heliconius butterflies, introgression was a major factor in their radiation, and the genetic variation it imparted into species is variable across the genome. Edelman et al. developed a new sequencing strategy and produced 20 Heliconius genomes (see the Perspective by Rieseberg). They also developed a means by which to identify genetic variation that originates from incomplete lineage sorting versus hybridization. Applying this model to their newly developed genomes, they investigated the evolutionary history of the genus and, in particular, the impact of introgression.
Science, this issue p. 594; see also p. 570.
We used 20 de novo genome assemblies to probe the speciation history and architecture of gene flow in rapidly radiating Heliconius butterflies. Our tests to distinguish incomplete lineage sorting from introgression indicate that gene flow has obscured several ancient phylogenetic relationships in this group over large swathes of the genome. Introgressed loci are underrepresented in low-recombination and gene-rich regions, consistent with the purging of foreign alleles more tightly linked to incompatibility loci. Here, we identify a hitherto unknown inversion that traps a color pattern switch locus. We infer that this inversion was transferred between lineages by introgression and is convergent with a similar rearrangement in another part of the genus. These multiple de novo genome sequences enable improved understanding of the importance of introgression and selective processes in adaptive radiation.
%B Science
%V 366
%P 594-599
%G eng
%U http://science.sciencemag.org/cgi/content/full/366/6465/594?ijkey=e55G0oV8OAoLY&keytype=ref&siteid=sci
%N November 1
%0 Journal Article
%J Zootaxa
%D 2019
%T Reply to Andrew Brower’s critique of the evidence for hybridization among Heliconius butterfly species in the wild
%A Mallet, James
%X Andrew Brower recently published a long article in this journal that seeks to dismantle evidence for hybridization between species of Heliconius butterflies. The main evidence that Brower criticizes here is given in two papers published by my colleagues and myself in 2007. In this reply, I briefly defend our evidence, and at greater length provide additional background information to help establish the credibility of the evidence even more firmly than previously
%B Zootaxa
%V 4679
%P 577-595
%G eng
%U http://dx.doi.org/10.11646/zootaxa.4679.3.11
%0 Journal Article
%J Evolution
%D 2019
%T Geographic contrasts between pre‐ and postzygotic barriers are consistent with reinforcement in Heliconius butterflies
%A Rosser, Neil
%A Queste, Lucie M.
%A Cama, Bruna
%A Nathaniel B. Edelman
%A Mann, Florian
%A Mori Pezo, Ronald
%A Morris, Jake
%A Segami, Carolina
%A Velado, Partricia
%A Schulz, Stefan
%A Mallet, James L.B.
%A Dasmahapatra, Kanchon K.
%X Identifying the traits causing reproductive isolation and the order in which they evolve is fundamental to understanding speciation. Here, we quantify prezygotic and intrinsic postzygotic isolation among allopatric, parapatric, and sympatric populations of the butterflies Heliconius elevatus and Heliconius pardalinus. Sympatric populations from the Amazon (H. elevatus and H. p. butleri) exhibit strong prezygotic isolation and rarely mate in captivity; however, hybrids are fertile. Allopatric populations from the Amazon (H. p. butleri) and Andes (H. p. sergestus) mate freely when brought together in captivity, but the female F1 hybrids are sterile. Parapatric populations (H. elevatus and H. p. sergestus) exhibit both assortative mating and sterility of female F1s. Assortative mating in sympatric populations is consistent with reinforcement in the face of gene flow, where the driving force, selection against hybrids, is due to disruption of mimicry and other ecological traits rather than hybrid sterility. In contrast, the lack of assortative mating and hybrid sterility observed in allopatric populations suggests that geographic isolation enables the evolution of intrinsic postzygotic reproductive isolation. Our results show how the types of reproductive barriers that evolve between species may depend on geography
%B Evolution
%V 73
%P 1821-1838
%G eng
%U https://doi.org/10.1111/evo.13804
%N 9
%0 Journal Article
%J Global Ecology and Biogeography
%D 2019
%T Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation
%A Chazot, Nicolas
%A Willmott, Keith R.
%A Lamas, Gerardo
%A Freitas, André V.L.
%A Piron-Prunier, Florence
%A Arias, Carlos F.
%A Mallet, James
%A de Silva, Donna Lisa
%A Elias, Marianne
%X
Aim The landscape of the Neotropical region has undergone dynamic evolution throughout the Miocene, with the extensive Pebas wetland occupying western Amazonia between 23 and c. 10 Ma and the continuous uplift of the Andes mountains. The complex interaction between the Andes and Amazonia probably influenced the trajectory of Neotropical biodiversity, but evidence from time-calibrated phylogenies of groups that diversified during this period is lacking. We investigate the role of these landscape transformations in the dynamics of diversification in the Neotropical region using a 26-Myr-old endemic butterfly radiation. Location Neotropics. Time period Oligocene to present. Major taxa studied Ithomiini butterflies.
Methods We generated one of the most comprehensive time-calibrated molecular phylogenies of a large clade of Neotropical insects, the butterfly tribe Ithomiini, comprising 340 species (87% of extant species) and spanning 26 Myr of diversification. We applied a large array of birth–death models and historical biogeography estimations to assess the dynamics of diversification and biotic interchanges, especially at the Amazonia–Andes interface.
Results Our results suggest that the Amazonian Pebas wetland system played a major role in the timing and geography of diversification of Ithomiini, by constraining dispersal and diversification in the Amazon basin until c. 10 Ma. During the Pebas wetland period, Ithomiini diversification mostly took place in the Andes, where terrestrial habitats were not affected. An explosion of interchanges with Amazonia and with the Northern Andes accompanied the demise of the Pebas system (11–8 Ma) and was followed by local diversification in those areas, which led to a substantial renewal of diversification.
Main conclusions Many studies on Neotropical diversity have focused only on the Andes, whereas we show that it is the waxing and waning of the Pebas mega-wetland, interacting with Andean uplift, that determined the timing and patterns of regional interchanges and diversification in Ithomiini.
%B Global Ecology and Biogeography
%V 28
%P 1118–1132.
%G eng
%U https://doi.org/10.1111/geb.12919
%N 8
%0 Journal Article
%J Genome Biology and Evolution
%D 2019
%T Simultaneous TE analysis of 19 heliconiine butterflies yields novel insights into rapid TE-based genome diversification and multiple SINE births and deaths
%A Ray, D. A.
%A Grimshaw, J.R.
%A Halsey, M.K.
%A Korstian, J.M.
%A Osmanski, A.B.
%A Sullivan, K.A.
%A Wolf, K.A.
%A Reddy, H.
%A Foley, N.
%A Stevens, R.D.
%A Knisbacher, B.
%A Levy, O.
%A Counterman, B.
%A Edelman, N.B.
%A Mallet, J.
%X Transposable elements (TEs) play major roles in the evolution of genome structure and function. However, because of their repetitive nature, they are difficult to annotate and discovering the specific roles they may play in a lineage can be a daunting task. Heliconiine butterflies are models for the study of multiple evolutionary processes including phenotype evolution and hybridization. We attempted to determine how TEs may play a role in the diversification of genomes within this clade by performing a detailed examination of TE content and accumulation in 19 species whose genomes were recently sequenced. We found that TE content has diverged substantially and rapidly in the time since several subclades shared a common ancestor with each lineage harboring a unique TE repertoire. Several novel SINE lineages have been established that are restricted to a subset of species. Furthermore, the previously described SINE, Metulj, appears to have gone extinct in two subclades while expanding to significant numbers in others. This diversity in TE content and activity has the potential to impact how heliconiine butterflies continue to evolve and diverge
%B Genome Biology and Evolution
%V 11
%P 2162-2177
%8 04 apr 2019
%G eng
%U https://doi.org/10.1093/gbe/evz125
%N 8
%0 Journal Article
%J Heredity
%D 2019
%T The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution
%A Morris, Jake
%A Navarro, Nicolas
%A Rastas, Pasi
%A Rawlins, Lauren D.
%A Sammy, Joshua
%A Mallet, James
%A Dasmahapatra, Kanchon K.
%B Heredity
%V 123
%P 138-152
%G eng
%U https://doi.org/10.1038/s41437-018-0180-0
%0 Journal Article
%J Zoological Journal of the Linnean Society
%D 2019
%T Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies
%A Rosser, N.
%A Freitas, A.V.L.
%A Huertas, B.
%A Joron, M.
%A Lamas, G.
%A Mérot, C.
%A Simpson, F.
%A Willmott, K.
%A Mallet, J.
%A Dasmahapatra, K. K.
%X
The evolution of reproductive isolation via a switch in mimetic wing coloration has become the paradigm for speciation in aposematic Heliconius butterflies. Here, we provide a counterexample to this, by documenting two cryptic species within the taxon formerly considered Heliconius demeter Staudinger, 1897. Amplified fragment length polymorphisms identify two sympatric genotypic clusters in northern Peru, corresponding to subspecies Heliconius demeter ucayalensis H. Holzinger & R. Holzinger, 1975 and Heliconius demeter joroni ssp. nov. These subspecies are reciprocally monophyletic for the mitochondrial genes COI and COII and the nuclear gene Ef1α, and exhibit marked differences in larval morphology and host plant use. COI sequences from 13 of the 15 currently recognized subspecies show that mtDNA differences are reflected across the range of H. demeter, with a deep phylogenetic split between the southern and northern Amazonian races. As such, our data suggest vicariant speciation driven by disruptive selection for larval performance on different host plants. We raise Heliconius demeter eratosignis (Joicey & Talbot, 1925) to Heliconius eratosignis based on nomenclatural priority, a species also comprising H. eratosignis ucayalensis comb. nov. and three other southern Amazonian races. Heliconius demeter joroni spp. nov. remains within H. demeter s.s., along with northern Amazonian and Guianan subspecies.
%B Zoological Journal of the Linnean Society
%V 186
%P 233-249
%G eng
%U https://doi.org/10.1093/zoolinnean/zly046
%N 1
%0 Report
%D 2018
%T Comments on petition of Pacific Legal Foundation, et al., for rule-making under the Administrative Procedure Act (which aimed to promulgate new regulatory definitions of “species” and “subspecies” under the Endangered Species Act)
%A Mallet, James
%A Ehrlich, Paul
%A Gill, Frank B.
%A McCormack, John
%A Raven, Peter
%A Chan, Shirley
%A Goho, Shaun A.
%G eng
%0 Journal Article
%J Current Biology
%D 2018
%T Supergene evolution triggered by the introgression of a chromosomal inversion
%A Jay, Paul
%A Whibley, Annabel
%A Frézal, Lise
%A de Cara, María Ángeles Rodríguez
%A Nowell, Reuben W.
%A Mallet, James
%A Dasmahapatra, Kanchon D.
%A Joron, Mathieu
%X Supergenes are groups of tightly linked loci whose variation is inherited as a single Mendelian locus and are a common genetic architecture for complex traits under balancing selection [1–8]. Supergene alleles are long-range haplotypes with numerous mutations underlying distinct adaptive strategies, often maintained in linkage disequilibrium through the suppression of recombination by chromosomal rearrangements [1, 5, 7–9]. However, the mechanism governing the formation of supergenes is not well understood and poses the paradox of establishing divergent functional haplotypes in the face of recombination. Here, we show that the formation of the supergene alleles encoding mimicry polymorphism in the butterfly Heliconius numata is associated with the introgression of a divergent, inverted chromosomal segment. Haplotype divergence and linkage disequilibrium indicate that supergene alleles, each allowing precisewing-pattern resemblance to distinct butterfly models, originate fromover a million years of independent chromosomal evolution in separate lineages. These ‘‘superalleles’’ have evolved from a chromosomal inversion captured by introgression and maintained in balanced polymorphism, triggering supergene inheritance. This mode of evolution involving the introgression of a chromosomal rearrangement is likely to be a common feature of complex structural polymorphisms associated with the coexistence of distinct adaptive syndromes. This shows that the reticulation of genealogies may have a powerful influence on the evolution of genetic architectures in nature.
%B Current Biology
%V 28
%P 1839-1845
%G eng
%U https://doi.org/10.1016/j.cub.2018.04.072
%0 Journal Article
%J Proceedings of the National Academy of Sciences
%D 2018
%T Invasive insect hybridizes with local pests
%A Mallet, James
%B Proceedings of the National Academy of Sciences
%V 115
%P 4819-4821
%G eng
%N 19
%0 Journal Article
%J Ecology and Evolution
%D 2018
%T Contrasting patterns of Andean diversification among three diverse clades of Neotropical clearwing butterflies
%A Chazot, N.
%A de Silva, D. L.
%A Willmott, K. R.
%A Freitas, A.V.L.
%A Lamas, G.
%A Mallet, J.
%A Giraldo, C.E.
%A Uribe, S.
%A Elias, M.
%B Ecology and Evolution
%V 8
%P 3965-3982
%G eng
%U https://doi.org/10.1002/ece3.3622
%N 8
%0 Journal Article
%J Tropical Lepidoptera Research
%D 2017
%T Review of: "The Ecology and Evolution of Heliconius Butterflies," by Chris D. Jiggins (2016)
%A Mallet, J.
%B Tropical Lepidoptera Research
%V 27
%P 120
%G eng
%N 2
%0 Journal Article
%J Nature Ecology and Evolution
%D 2017
%T Complex modular architecture around a simple toolkit of wing pattern genes
%A Van Belleghem, S.M.
%A Rastas, P.
%A Papanicolaou, A.
%A Martin, S. H.
%A Arias, C.F.
%A Supple, M.A.
%A Hanly, J.J.
%A Mallet, J.
%A Lewis, J.J.
%A Hines, H. M.
%A Ruiz, M.
%A Salazar, C.
%A Linares, M.
%A Moreira, G.R.P.
%A Jiggins, C. D.
%A Counterman, B. A.
%A McMillan, W. O.
%A Papa, R.
%B Nature Ecology and Evolution
%V 1
%P 0052
%8 30 Jan 2017
%G eng
%U http://dx.doi.org/10.1038/s41559-016-0052
%0 Journal Article
%J Scientific Reports
%D 2017
%T North Andean origin and diversification of the largest ithomiine butterfly genus [Pteronymia]
%A de Silva, Donna Lisa
%A Mota, Luísa L.
%A Chazot, Nicolas
%A Mallarino, Ricardo
%A Silva-Brandão, Karina L.
%A Gómez Piñerez, Luz Miryam
%A Freitas, André V.L.
%A Lamas, Gerardo
%A Joron, Mathieu
%A Mallet, James
%A Giraldo, Carlos E.
%A Uribe, Sandra
%A Särkinen, Tiina
%A Knapp, Sandra
%A Jiggins, Chris D.
%A Willmott, Keith R.
%A Elias, Marianne
%X
Article |OPEN
North Andean origin and diversification of the largest ithomiine butterfly genus
The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genusPteronymia(Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, makingPteronymiathe most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows thatPteronymiaoriginated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species’ elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed toPteronymiadiversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others
%B Scientific Reports
%V 7
%P 45966
%G eng
%U https://doi.org/10.1038/srep45966
%0 Journal Article
%J Molecular Ecology
%D 2016
%T Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina
%A Chazot, N.
%A Willmott, K. R.
%A Condamine, F. L.
%A de Silva, D. L.
%A Freitas, A.V.L.
%A Morlon, H.
%A Giraldo, C.E.
%A Jiggins, C. D.
%A Joron, M.
%A Mallet, J.
%A Uribe, S.
%A Elias, M.
%X
Understanding why species richness peaks along the Andes is a fundamental question in the study of Neotropical biodiversity. Several biogeographic and diversification scenarios have been proposed in the literature, but there is confusion about the processes underlying each scenario, and assessing their relative contribution is not straightforward. Here, we propose to refine these scenarios into a framework which evaluates four evolutionary mechanisms: higher speciation rate in the Andes, lower extinction rates in the Andes, older colonization times and higher colonization rates of the Andes from adjacent areas. We apply this framework to a species-rich subtribe of Neotropical butterflies whose diversity peaks in the Andes, the Godyridina (Nymphalidae: Ithomiini). We generated a time-calibrated phylogeny of the Godyridina and fitted time-dependent diversification models. Using trait-dependent diversification models and ancestral state reconstruction methods we then compared different biogeographic scenarios. We found strong evidence that the rates of colonization into the Andes were higher than the other way round. Those colonizations and the subsequent local diversification at equal rates in the Andes and in non-Andean regions mechanically increased the species richness of Andean regions compared to that of non-Andean regions (‘species-attractor’ hypothesis). We also found support for increasing speciation rates associated with Andean lineages. Our work highlights the importance of the Andean slopes in repeatedly attracting non-Andean lineages, most likely as a result of the diversity of habitats and/or host plants. Applying this analytical framework to other clades will bring important insights into the evolutionary mechanisms underlying the most species-rich biodiversity hotspot on the planet.
%B Molecular Ecology
%V 25
%P 5765-5784
%G eng
%U http://onlinelibrary.wiley.com/wol1/doi/10.1111/mec.13773/full
%N 22
%0 Journal Article
%J Conservación Colombiana
%D 2016
%T A remarkable new butterfly species from western Amazonia (Lepidoptera: Nymphalidae: Satyrinae).
%A Huertas, B..
%A Lamas, G.
%A Fagua, G.
%A Mallet, J.
%A Nakahara, S.
%A Willmott, K.
%B Conservación Colombiana
%V 24
%P 5-11
%G eng
%U http://www.proaves.org/wp-content/uploads/2016/11/Nueva-especie-de-mariposa-Cons-Col-24-5-11-Huertas-et-al.pdf
%0 Journal Article
%J Current Biology
%D 2016
%T Ecological genetics: a key gene for mimicry and melanism
%A Mallet, J.
%A Hoekstra, H. E.
%X
The major revolution in Charles Darwin’s ‘On the Origin of Species’ was the proposal that evolutionary change took place by natural selection. The ‘Origin’ was highly influential primarily because of its convincing, logical arguments, but in 1859 Darwin was unable to provide a single empirical case of natural selection. By the late 19th century, two key examples of natural selection became known: mimicry in heliconian butterflies and rapid increases in melanic forms of the peppered moth (Biston betularia) as well as of many other moth species in industrial Britain [1, 2]. Only now, however, are we beginning to catch a glimpse of the genetics underlying these adaptive changes. Remarkably, two independent and different-looking colour pattern switches in Lepidoptera — one in wing colour patterning and one that melanizes all scales over the wings and body — have been mapped to exactly the same gene in Heliconius and Biston [3, 4].
%B Current Biology
%V 26
%P R802-R804
%G eng
%N 17
%0 Journal Article
%J PLoS Genetics
%D 2016
%T What is speciation?
%A Shapiro,B.J.
%A Le Ducq,J.B.
%A Mallet, J.
%X
Concepts and definitions of species have been debated by generations of biologists and remain controversial. Microbes pose a particular challenge because of their genetic diversity, asexual reproduction, and often promiscuous horizontal gene transfer (HGT). However, microbes also present an opportunity to study and understand speciation because of their rapid evolution, both in nature and in the lab, and small, easily sequenced genomes. Here, we review how microbial population genomics has enabled us to catch speciation ?in the act? and how the results have challenged and enriched our concepts of species, with implications for all domains of life. We describe how recombination (including HGT and introgression) has shaped the genomes of nascent microbial, animal, and plant species and argue for a prominent role of natural selection in initiating and maintaining speciation. We ask how universal is the process of speciation across the tree of life, and what lessons can be drawn from microbes? Comparative genomics showing the extent of HGT in natural populations certainly jeopardizes the relevance of vertical descent (i.e., the species tree) in speciation. Nevertheless, we conclude that species do indeed exist as clusters of genetic and ecological similarity and that speciation is driven primarily by natural selection, regardless of the balance between horizontal and vertical descent.
%B PLoS Genetics
%V 12
%P e1005860
%G eng
%U http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1005860
%N 3
%0 Journal Article
%J G3: Genes, Genomes, Genetics
%D 2016
%T Major improvements to the Heliconius melpomene genome assembly used to confirm 10 chromosome fusion events in 6 million years of butterfly evolution
%A Davey, J. W.
%A Chouteau, M.
%A Barker, S.L.
%A Maroja, L.
%A Baxter, S. W.
%A Simpson, F.
%A Merrill, R. M.
%A Joron, M.
%A Mallet, J.
%A Dasmahapatra, K. K.
%A Jiggins, C. D.
%X
The Heliconius butterflies are a widely studied adaptive radiation of 46 species spread across Central and South America, several of which are known to hybridize in the wild. Here, we present a substantially improved assembly of the Heliconius melpomene genome, developed using novel methods that should be applicable to improving other genome assemblies produced using short read sequencing. First, we whole-genome-sequenced a pedigree to produce a linkage map incorporating 99% of the genome. Second, we incorporated haplotype scaffolds extensively to produce a more complete haploid version of the draft genome. Third, we incorporated ∼20x coverage of Pacific Biosciences sequencing, and scaffolded the haploid genome using an assembly of this long-read sequence. These improvements result in a genome of 795 scaffolds, 275 Mb in length, with an N50 length of 2.1 Mb, an N50 number of 34, and with 99% of the genome placed, and 84% anchored on chromosomes. We use the new genome assembly to confirm that the Heliconius genome underwent 10 chromosome fusions since the split with its sister genusEueides, over a period of about 6 million yr.
%B G3: Genes, Genomes, Genetics
%V 6
%P 695-708
%G eng
%U http://www.g3journal.org/content/6/3/695
%N 3
%0 Journal Article
%J Genome Biology
%D 2016
%T Genome-wide introgression among distantly related Heliconius butterfly species
%A Zhang, W.
%A Dasmahapatra, K.
%A Mallet, J.
%A Moreira, G.
%A Kronforst, M.
%X
BACKGROUND:
Although hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation. The butterfly genus Heliconius is an excellent system to study hybridization and introgression but most studies have focused on closely related species such as H. cydno and H. melpomene. Here we characterize genome-wide patterns of introgression between H. besckei, the only species with a red and yellow banded 'postman' wing pattern in the tiger-striped silvaniform clade, and co-mimetic H. melpomene nanna.
RESULTS:
We find a pronounced signature of putative introgression from H. melpomene into H. besckei in the genomic region upstream of the gene optix, known to control red wing patterning, suggesting adaptive introgression of wing pattern mimicry between these two distantly related species. At least 39 additional genomic regions show signals of introgression as strong or stronger than this mimicry locus. Gene flow has been on-going, with evidence of gene exchange at multiple time points, and bidirectional, moving from the melpomene to the silvaniform clade and vice versa. The history of gene exchange has also been complex, with contributions from multiple silvaniform species in addition to H. besckei. We also detect a signature of ancient introgression of the entire Z chromosome between the silvaniform and melpomene/cydno clades.
CONCLUSIONS:
Our study provides a genome-wide portrait of introgression between distantly related butterfly species. We further propose a comprehensive and efficient workflow for gene flow identification in genomic data sets.
%B Genome Biology
%V 17
%G eng
%N 25
%0 Journal Article
%J PloS Biology
%D 2016
%T The origins of an evolutionary novelty through enhancer shuffling
%A Wallbank, R.W.R.
%A Baxter, S.
%A Pardo-Diaz, C.
%A Hanly, J.J.
%A Martin, S. H.
%A Mallet, J.
%A Dasmahapatra, K. K.
%A Salazar, C.
%A Joron, M.
%A Nadeau, N.
%A McMillan, W. O.
%A Jiggins, C. D.
%X
An important goal in evolutionary biology is to understand the genetic changes underlying novel morphological structures. We investigated the origins of a complex wing pattern found among Amazonian Heliconius butterflies. Genome sequence data from 142 individuals across 17 species identified narrow regions associated with two distinct red colour pattern elements, dennis and ray. We hypothesise that these modules in non-coding sequence represent distinct cis-regulatory loci that control expression of the transcription factor optix, which in turn controls red pattern variation across Heliconius. Phylogenetic analysis of the two elements demonstrated that they have distinct evolutionary histories and that novel adaptive morphological variation was created by shuffling these cis-regulatory modules through recombination between divergent lineages. In addition, recombination of modules into different combinations within species further contributes to diversity. Analysis of the timing of diversification in these two regions supports the hypothesis of introgression moving regulatory modules between species, rather than shared ancestral variation. The dennis phenotype introgressed into Heliconius melpomene at about the same time that ray originated in this group, while ray introgressed back into H. elevatus much more recently. We show that shuffling of existing enhancer elements both within and between species provides a mechanism for rapid diversification and generation of novel morphological combinations during adaptive radiation.
%B PloS Biology
%V 14
%P e1002353
%G eng
%N 1
%0 Journal Article
%J BioEssays
%D 2016
%T How reticulated are species?
%A Mallet, J.
%A Besansky, N.
%A Hahn, M.W.
%X
Many groups of closely related species have reticulate phylogenies. Recent
genomic analyses are showing this in many insects and vertebrates, as well as in microbes and plants. In microbes, lateral gene transfer is the dominant
process that spoils strictly tree-like phylogenies, but in multicellular eukaryotes hybridization and introgression among related species is probably more important. Because many species, including the ancestors of ancient major lineages, seem to evolve rapidly in adaptive radiations, some sexual compatibility may exist among them. Introgression and reticulation can thereby affect all parts of the tree of life, not just the recent species at the tips. Our understanding of adaptive evolution, speciation, phylogenetics, and comparative biology must adapt to these mostly recent findings. Introgression has important practical implications as well, not least for the management of genetically modified organisms in pest and disease control.
%B BioEssays
%V 38
%P 140-149
%8 2016
%G eng
%N 2
%0 Journal Article
%J Journal of Biogeography
%D 2016
%T Diversification of clearwing butterflies with the rise of the Andes
%A de Silva, D. L.
%A Elias, M.
%A Willmott, K.
%A Mallet, J.
%A Day, J. J.
%K Andes, biogeography, diversification, ecological speciation, Hyposcada, Ithomiini butterflies, Megoleria, Neotropics, Oleria, Ollantaya.
%X
Despite the greatest butterfly diversity on Earth occurring in the Neotropical Andes and Amazonia, there is still keen debate about the origins of this exceptional biota. A densely sampled calibrated phylogeny for a widespread butterfly subtribe, Oleriina (Ithomiini: Nymphalidae) was used to estimate the origin, colonization history and diversification of this species-rich group.
%B Journal of Biogeography
%V 43
%P 44-58
%G eng
%U http://dx.doi.org/10.1111/jbi.12611
%0 Journal Article
%J BMC Evolutionary Biology
%D 2015
%T Extensive range overlap between Heliconius sister species: evidence for sympatric speciation in butterflies?
%A Rosser, N.
%A Phillimore, A. B.
%A Mallet, J.
%X
Background
Sympatric speciation is today generally viewed as plausible, and some well-supported examples exist, but its relative contribution to biodiversity remains to be established. We here quantify geographic overlap of sister species of heliconiine butterflies, and use age-range correlations and spatial simulations of the geography of speciation to infer the frequency of sympatric speciation. We also test whether shifts in mimetic wing colour pattern, host plant use and climate niche play a role in speciation, and whether such shifts are associated with sympatry.
Results
Approximately a third of all heliconiine sister species pairs exhibit near complete range overlap, and analyses of the observed patterns of range overlap suggest that sympatric speciation contributes 32 %–95 % of speciation events. Müllerian mimicry colour patterns and host plant choice are highly labile traits that seem to be associated with speciation, but we find no association between shifts in these traits and range overlap. In contrast, climatic niches of sister species are more conserved.
Conclusions
Unlike birds and mammals, sister species of heliconiines are often sympatric and our inferences using the most recent comparative methods suggest that sympatric speciation is common. However, if sister species spread rapidly into sympatry (e.g. due to their similar climatic niches), then assumptions underlying our methods would be violated. Furthermore, although we find some evidence for the role of ecology in speciation, ecological shifts did not show the associations with range overlap expected under sympatric speciation. We delimit species of heliconiines in three different ways, based on “strict and ” “relaxed” biological species concepts (BSC), as well as on a surrogate for the widely-used “diagnostic” version of the phylogenetic species concept (PSC). We show that one reason why more sympatric speciation is inferred in heliconiines than in birds may be due to a different culture of species delimitation in the two groups. To establish whether heliconiines are exceptional will require biogeographic comparative studies for a wider range of animal taxa including many more invertebrates.
%B BMC Evolutionary Biology
%V 15
%P 125
%G eng
%U https://dx.doi.org/10.1186/s12862-015-0420-3
%0 Journal Article
%J Molecular Biology and Evolution
%D 2015
%T Estimation of the spontaneous mutation rate in Heliconius melpomene
%A Keightley, P. D.
%A Pinharanda, A.
%A Ness, R. W.
%A Simpson, F.
%A Dasmahapatra, K. K.
%A Mallet, J.
%A Davey, J. W.
%A Jiggins, C. D.
%K genome sequencing
%K Heliconius
%K Mutation
%X
We estimated the spontaneous mutation rate in Heliconius melpomene by genome sequencing of a pair of parents and 30 of their offspring, based on the ratio of number of de novo heterozygotes to the number of callable site-individuals. We detected nine new mutations, each one affecting a single site in a single offspring. This yields an estimated mutation rate of 2.9 x 10(-9) (95% confidence interval, 1.3 x 10(-9)-5.5 x 10(-9)), which is similar to recent estimates in Drosophila melanogaster, the only other insect species in which the mutation rate has been directly estimated. We infer that recent effective population size of H. melpomene is about 2 million, a substantially lower value than its census size, suggesting a role for natural selection reducing diversity. We estimate that H. melpomene diverged from its Mullerian comimic H. erato about 6 Ma, a somewhat later date than estimates based on a local molecular clock.
%B Molecular Biology and Evolution
%V 32
%P 239-43
%8 Jan
%@ 1537-1719 (Electronic)0737-4038 (Linking)
%G eng
%U http://dx.doi.org/10.1093/molbev/msu302
%M 25371432
%2 4271535
%0 Journal Article
%J Systematic Biology
%D 2015
%T Multilocus species trees show the recent adaptive radiation of the mimetic Heliconius butterflies
%A Kozak, K. M.
%A Wahlberg, N.
%A Neild, A. F.
%A Dasmahapatra, K. K.
%A Mallet, J.
%A Jiggins, C. D.
%K Amazonia
%K diversification rate
%K incongruence
%K lepidoptera
%K mimicry
%K Miocene
%K multispecies coalescent
%X
Mullerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification. We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.
For over 100 years, it has been known that polymorphic mimicry is often switched by simple mendelian factors, yet the physical nature of these loci had escaped characterization. Now, the genome sequences of two swallowtail butterfly (Papilio) species have enabled the precise identification of a locus underlying mimicry, adding to unprecedented recent discoveries in mimicry genetics.
%B Nature Genetics
%V 47
%P 306-7
%8 Apr
%@ 1546-1718 (Electronic)1061-4036 (Linking)
%G eng
%M 25814305
%0 Journal Article
%J Current Biology
%D 2014
%T Speciation: frog mimics prefer their own
%A Mallet, J.
%X
Ranitomeya poison frogs in the Peruvian Amazon are a rare example of Mullerian mimicry in vertebrates. These frogs also prefer to court same-coloured mimics. This suggests that divergence in mimicry plays a role in reproductive isolation.
%B Current Biology
%V 24
%P R1094-R1096
%8 Nov 17
%@ 1879-0445 (Electronic)0960-9822 (Linking)
%G eng
%M 25458221
%0 Journal Article
%J Evolution
%D 2014
%T Stable Heliconius butterfly hybrid zones are correlated with a local rainfall peak at the edge of the Amazon basin
%A Rosser, N.
%A Dasmahapatra, K. K.
%A Mallet, J.
%K Frequency-dependent selection
%K Heliconius butterflies
%K mimicry
%K moving hybrid zones
%K Pleistocene refugia
%X
Multilocus clines between Mullerian mimetic races of Heliconius butterflies provide a classic example of the maintenance of hybrid zones and their importance in speciation. Concordant hybrid zones in the mimics Heliconius erato and H. melpomene in northern Peru were carefully documented in the 1980s, and this prior work now permits a historical analysis of the movement or stasis of the zones. Previous work predicted that these zones might be moving toward the Andes due to selective asymmetry. Extensive deforestation and climate change might also be expected to affect the positions and widths of the hybrid zones. We show that the positions and shapes of these hybrid zones have instead remained remarkably stable between 1985 and 2012. The stability of this interaction strongly implicates continued selection, rather than neutral mixing following secondary contact. The stability of cline widths and strong linkage disequilibria (gametic correlation coefficients Rmax = 0.35-0.56 among unlinked loci) over 25 years suggest that mimetic selection pressures on each color pattern locus have remained approximately constant (s approximately 0.13-0.40 per locus in both species). Exceptionally high levels of precipitation at the edge of the easternmost Andes may act as a population density trough for butterflies, trapping the hybrid zones at the foot of the mountains, and preventing movement. As such, our results falsify one prediction of the Pleistocene Refugium theory: That the ranges of divergent species or subspecies should be centered on regions characterized by maxima of rainfall, with hybrid zones falling in more arid regions between them.
%B Evolution
%V 68
%P 3470-3484
%8 Dec
%@ 1558-5646 (Electronic)0014-3820 (Linking)
%G eng
%U http://dx.doi.org/10.1111/evo.12539
%M 25311415
%0 Journal Article
%J Biological Journal of the Linnean Society
%D 2013
%T Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae).
%A Mérot,C
%A Mavárez, J
%A Evin, A
%A Dasmahapatra, K. K.
%A Mallet, J.
%A Lamas, G.
%A Joron, M.
%K geometric morphometrics
%K hybridization
%K multilocus genotype
%K reproductive isolation
%K Speciation
%K wing shape.
%X
%B Biological Journal of the Linnean Society
%V 109
%P 830-847
%G eng
%0 Journal Article
%J eratosignis
%D 2013
%T Introgression: Brower's criticisms. Part I. New evidence for hybridization and introgression is unsettling.
%A Mallet, James
%B eratosignis
%G eng
%U www.heliconius.org
%0 Journal Article
%J eratosignis
%D 2013
%T Introgression: Brower's criticisms. Part II. Itemized critiques by Brower (2012), and comments thereon
%A Mallet, James
%B eratosignis
%G eng
%U www.heliconius.org
%0 Journal Article
%J Journal of Evolutionary Biology
%D 2013
%T Ecological and genetic factors influencing the transition between host-use strategies in sympatric Heliconius butterflies
%A Merrill, R. M.
%A Naisbit, R. E.
%A Mallet, J.
%A Jiggins, C. D.
%K *Ecosystem
%K *Selection, Genetic
%K Animals
%K Butterflies/*genetics/physiology
%K coexistence
%K Competitive Behavior/*physiology
%K Genetic Association Studies
%K Genetic Linkage
%K host-plant use
%K Larva/physiology
%K lepidoptera
%K Panama
%K Passiflora/*parasitology
%K Pigmentation/*physiology
%K Speciation
%K Species Specificity
%K survival analysis
%X
Shifts in host-plant use by phytophagous insects have played a central role in their diversification. Evolving host-use strategies will reflect a trade-off between selection pressures. The ecological niche of herbivorous insects is partitioned along several dimensions, and if populations remain in contact, recombination will break down associations between relevant loci. As such, genetic architecture can profoundly affect the coordinated divergence of traits and subsequently the ability to exploit novel habitats. The closely related species Heliconius cydno and H. melpomene differ in mimetic colour pattern, habitat and host-plant use. We investigate the selection pressures and genetic basis underlying host-use differences in these two species. Host-plant surveys reveal that H. melpomene specializes on a single species of Passiflora. This is also true for the majority of other Heliconius species in secondary growth forest at our study site, as expected under a model of interspecific competition. In contrast, H. cydno, which uses closed-forest habitats where both Heliconius and Passiflora are less common, appears not to be restricted by competition and uses a broad selection of the available Passiflora. However, other selection pressures are likely involved, and field experiments reveal that early larval survival of both butterfly species is highest on Passiflora menispermifolia, but most markedly so for H. melpomene, the specialist on that host. Finally, we demonstrate an association between host-plant acceptance and colour pattern amongst interspecific hybrids, suggesting that major loci underlying these important ecological traits are physically linked in the genome. Together, our results reveal ecological and genetic associations between shifts in habitat, host use and mimetic colour pattern that have likely facilitated both speciation and coexistence.
%B Journal of Evolutionary Biology
%V 26
%P 1959-67
%8 Sep
%@ 1420-9101 (Electronic)1010-061X (Linking)
%G eng
%M 23961921
%0 Journal Article
%J PLoS Genetics
%D 2013
%T Female behaviour drives expression and evolution of gustatory receptors in butterflies
%A Briscoe, A. D.
%A Macias-Munoz, A.
%A Kozak, K. M.
%A Walters, J. R.
%A Yuan, F.
%A Jamie, G. A.
%A Martin, S. H.
%A Dasmahapatra, K. K.
%A Ferguson, L. C.
%A Mallet, J.
%A Jacquin-Joly, E.
%A Jiggins, C. D.
%K *Feeding Behavior
%K *Gene Duplication
%K Animals
%K Butterflies/*genetics/physiology
%K DNA Copy Number Variations/*genetics
%K Drosophila Proteins/genetics
%K Evolution, Molecular
%K Female
%K Genome, Insect
%K Male
%K Oviposition/genetics
%K Phylogeny
%K Receptors, Cell Surface/genetics
%K Taste Perception/*genetics
%X
Secondary plant compounds are strong deterrents of insect oviposition and feeding, but may also be attractants for specialist herbivores. These insect-plant interactions are mediated by insect gustatory receptors (Grs) and olfactory receptors (Ors). An analysis of the reference genome of the butterfly Heliconius melpomene, which feeds on passion-flower vines (Passiflora spp.), together with whole-genome sequencing within the species and across the Heliconius phylogeny has permitted an unprecedented opportunity to study the patterns of gene duplication and copy-number variation (CNV) among these key sensory genes. We report in silico gene predictions of 73 Gr genes in the H. melpomene reference genome, including putative CO2, sugar, sugar alcohol, fructose, and bitter receptors. The majority of these Grs are the result of gene duplications since Heliconius shared a common ancestor with the monarch butterfly or the silkmoth. Among Grs but not Ors, CNVs are more common within species in those gene lineages that have also duplicated over this evolutionary time-scale, suggesting ongoing rapid gene family evolution. Deep sequencing ( approximately 1 billion reads) of transcriptomes from proboscis and labial palps, antennae, and legs of adult H. melpomene males and females indicates that 67 of the predicted 73 Gr genes and 67 of the 70 predicted Or genes are expressed in these three tissues. Intriguingly, we find that one-third of all Grs show female-biased gene expression (n = 26) and nearly all of these (n = 21) are Heliconius-specific Grs. In fact, a significant excess of Grs that are expressed in female legs but not male legs are the result of recent gene duplication. This difference in Gr gene expression diversity between the sexes is accompanied by a striking sexual dimorphism in the abundance of gustatory sensilla on the forelegs of H. melpomene, suggesting that female oviposition behaviour drives the evolution of new gustatory receptors in butterfly genomes.
%B PLoS Genetics
%V 9
%P e1003620
%@ 1553-7404 (Electronic)1553-7390 (Linking)
%G eng
%M 23950722
%2 3732137
%0 Journal Article
%J Genome Research
%D 2013
%T Genome-wide evidence for speciation with gene flow in Heliconius butterflies
%A Martin, S. H.
%A Dasmahapatra, K. K.
%A Nadeau, N. J.
%A Salazar, C.
%A Walters, J. R.
%A Simpson, F.
%A Blaxter, M.
%A Manica, A.
%A Mallet, J.
%A Jiggins, C. D.
%K *Gene Flow
%K *Genes, Insect
%K *Genetic Speciation
%K *Sympatry
%K Alleles
%K Animals
%K Butterflies/classification/*genetics
%K Evolution, Molecular
%K Genetic Variation
%K genome
%K Genome, Insect
%K Linkage Disequilibrium
%K Phenotype
%K Phylogeny
%K Sex Chromosomes/genetics
%X
Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on whole-genome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mullerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.
%B Genome Research
%V 23
%P 1817-1828
%8 Nov
%@ 1549-5469 (Electronic)1088-9051 (Linking)
%G eng
%M 24045163
%2 3814882
%0 Journal Article
%J Journal of Evolutionary Biology
%D 2013
%T Hybridization and speciation
%A Abbott, R.
%A Albach, D.
%A Ansell, S.
%A Arntzen, J. W.
%A Baird, S. J.
%A Bierne, N.
%A Boughman, J.
%A Brelsford, A.
%A Buerkle, C. A.
%A Buggs, R.
%A Butlin, R. K.
%A Dieckmann, U.
%A Eroukhmanoff, F.
%A Grill, A.
%A Cahan, S. H.
%A Hermansen, J. S.
%A Hewitt, G.
%A Hudson, A. G.
%A Jiggins, C.
%A Jones, J.
%A Keller, B.
%A Marczewski, T.
%A Mallet, J.
%A Martinez-Rodriguez, P.
%A Most, M.
%A Mullen, S.
%A Nichols, R.
%A Nolte, A. W.
%A Parisod, C.
%A Pfennig, K.
%A Rice, A. M.
%A Ritchie, M. G.
%A Seifert, B.
%A Smadja, C. M.
%A Stelkens, R.
%A Szymura, J. M.
%A Vainola, R.
%A Wolf, J. B.
%A Zinner, D.
%K *Genetic Speciation
%K *Hybridization, Genetic
%K Adaptation, Physiological
%K Animals
%K Gene Flow
%K Phenotype
%X
Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.
%B Journal of Evolutionary Biology
%V 26
%P 229-246
%8 Feb
%@ 1420-9101 (Electronic)1010-061X (Linking)
%G eng
%M 23323997
%0 Journal Article
%J Biological Journal of the Linnean Society
%D 2012
%T Ecologically relevant cryptic species in the highly polymorphic Amazonian butterfly Mechanitismazaeus, sensu lato (Lepidoptera: Nymphalidae; Ithomiini).
%A Hill, R. I.
%A Elias, M.
%A Dasmahapatra, K. K.
%A Jiggins, C. D.
%A Koong, V.
%A Willmott, K. R.
%A Mallet, J.
%K Amazonia – biodiversity – DNA barcoding – host plant – integrative taxonomy
%K – Müllerian mimicry – mitochondrial DNA – Neotropics – Solanum.
%X
%B Biological Journal of the Linnean Society
%V 106
%P 540-560
%G eng
%0 Journal Article
%J Molecular Ecology
%D 2012
%T Hybrid zones and the speciation continuum in Heliconius butterflies.
%A Mallet, J.
%A Dasmahapatra, K. K.
%X
Tropical butterflies in the genus Heliconius have long 25 been models in26 the study of the stages of speciation. Heliconius are unpalatable to27 predators, and many species are notable for multiple geographic28 populations with striking warning colour pattern differences associated29 with Müllerian mimicry. There is a speciation continuum evident in30 Heliconius hybrid zones, across which mimicry patterns are often31 different, but where hybrids are common and little else differs, through32 to 'bimodal' hybrid zones with strongly marked molecular differences33 with few hybrids, through to 'good' sympatric species. Now Arias et al.34 (2012) have found an intermediate case in Colombian Heliconius cydno35 showing evidence for assortative mating and molecular differences, but36 where hybrids are abundant.
%B Molecular Ecology
%V 21
%P 5643-5645
%G eng
%0 Journal Article
%J Evolutionary Ecology Research
%D 2012
%T The struggle for existence. How the notion of carrying capacity, K, obscures the links between demography, Darwinian evolution and speciation.
%A Mallet, J.
%K adaptive dynamics, density-dependent selection, eco-evolutionary dynamics,
%K history of ecology, population genetics, theoretical ecology
%X
Question: Population ecology and population genetics are treated separately in mosttextbooks. However, Darwin’s term the ‘struggle for existence’ included both naturalselection and ecological competition. Using the simplest possible mathematical models, thispaper searches for historical reasons for the lack of unity in ecological and evolutionarythought.Assumptions and methods: Logistic density-dependent population growth and Lotka-Volterracompetition models are used throughout. Derivations of the logistic from first principles ofresource use, competition for space, and births and deaths of individuals are documented.A full range of possible kinds of natural selection, including constant selection, density- andfrequency-dependent selection, as well as hard and soft selection, can emerge cleanly asnatural outcomes from the simplest-imaginable haploid models derived from Lotka-Volterracompetition. Extensions to incorporate more realism, including non-linear per capita densitydependence, Allee effects, complex life histories, discrete generations, diploid Mendeliangenetics, sexual populations, and speciation are briefly discussed.Conclusions: Widespread use of r-K (‘carrying capacity’) models of population growthappears to have catalysed fundamental discords in ecology, and between ecology and evolution.Verhulst’s original polynomial form of the logistic, here termed the r-α model, is both morenatural in theory, and accords better with empirical data. The r-α formulation explainsapparent paradoxes involving the r-K logistic, including controversial aspects of r- andK-selection. Adoption of first-principles birth–death or r-α modelling clarifies natural selectionin density-regulated populations, and leads to an improved understanding of Darwinianevolution and speciation.
%B Evolutionary Ecology Research
%V 14
%P 627–665
%G eng
%0 Journal Article
%J Biological Journal of the Linnean Society
%D 2012
%T Testing historical explanations for gradients in species richness in heliconiine butterflies of tropical America.
%A Rosser, N.
%A Phillimore, A. B.
%A Huertas, B.
%A Willmott, K. R.
%A Mallet, J.
%K ange maps
%K conservatism
%K evolutionary age
%K extinction
%K Speciation
%K subspecies richness
%K suture zones
%K terminal phylogenetic branch length
%X
%B Biological Journal of the Linnean Society
%V 105
%P 479-497
%G eng
%0 Journal Article
%J Nature
%D 2012
%T Butterfly genome reveals promiscuous exchange of mimicry adaptations among species
%A Heliconius_Genome_Consortium
%K *Evolution, Molecular
%K Adaptation, Physiological/*genetics
%K Animals
%K Bombyx/genetics
%K Butterflies/*classification/*genetics
%K Chromosomes, Insect/genetics
%K Gene Flow
%K Genes, Homeobox/genetics
%K Genes, Insect/genetics
%K Genome, Insect/*genetics
%K Genomics
%K Hybridization, Genetic/genetics
%K Molecular Mimicry/*genetics
%K Molecular Sequence Data
%K Phylogeny
%K Pigmentation/genetics
%K Sequence Analysis, DNA
%K Species Specificity
%K Synteny/genetics
%K Wing/anatomy & histology
%X
The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.
%B Nature
%V 487
%P 94-98
%8 Jul 5
%@ 1476-4687 (Electronic)0028-0836 (Linking)
%G eng
%M 22722851
%2 3398145
%0 Journal Article
%J European Journal of Protistology
%D 2012
%T Concepts in protistology: species definitions and boundaries
%A Boenigk, J.
%A Ereshefsky, M.
%A Hoef-Emden, K.
%A Mallet, J.
%A Bass, D.
%K *Terminology as Topic
%K Eukaryota/*physiology
%K Species Specificity
%X
This paper summarises the Symposium 'Concepts in Protistology', during the VI European Congress of Protistology, Berlin, 25-29 July 2011. There is an increasing focus on cataloguing the number of species on earth, species barcoding initiatives, and the increasing need to reconcile molecular with morphological data in protists within a taxonomic framework. We identify several obstructions to defining species in protists, including the high incidence of asexuality, high levels of both morphological conservation and evolutionary convergence, high levels of genetic diversity that cannot so far be correlated with phenotypic characters, conflicting signals between both genetic and phenotypic taxonomic markers, and different requirements and challenges of species definition in different protist groups. We assert that there is no species 'category' for protists, and recommend that a working definition of species is clarified on a case-by-case basis. Thus, a consensus approach may emerge within protist groups, but any one approach is unlikely to encompass a wide phylogenetic range. However, as long as clarity of intent and method is maintained, the utility of the term 'species' in protists will also be maintained as a reproducible and convenient (if artificial) way of referring to particular lineages within a tightly defined context.
%B European Journal of Protistology
%V 48
%P 96-102
%8 May
%@ 1618-0429 (Electronic)0932-4739 (Linking)
%G eng
%M 22209540
%0 Journal Article
%J Proceedings of the Royal Society B: Biological Sciences
%D 2012
%T Disruptive ecological selection on a mating cue
%A Merrill, R. M.
%A Wallbank, R. W.
%A Bull, V.
%A Salazar, P. C.
%A Mallet, J.
%A Stevens, M.
%A Jiggins, C. D.
%K *Predatory Behavior
%K *Selection, Genetic
%K Animals
%K Birds/*physiology
%K Butterflies/genetics/*physiology
%K Color
%K Food Chain
%K Hybridization, Genetic
%K Mating Preference, Animal
%K Panama
%K Phenotype
%K Species Specificity
%X
Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such 'magic' or 'multiple-effect' traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Mullerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.
%B Proceedings of the Royal Society B: Biological Sciences
%V 279
%P 4907-4913
%8 Dec 22
%@ 1471-2954 (Electronic)0962-8452 (Linking)
%G eng
%M 23075843
%2 3497240
%0 Journal Article
%J Molecular Ecology
%D 2012
%T Genome-wide patterns of divergence and gene flow across a butterfly radiation
%A Nadeau, N. J.
%A Martin, S. H.
%A Kozak, K. M.
%A Salazar, C.
%A Dasmahapatra, K. K.
%A Davey, J. W.
%A Baxter, S. W.
%A Blaxter, M. L.
%A Mallet, J.
%A Jiggins, C. D.
%K *Gene Flow
%K *Genetic Speciation
%K *Phylogeny
%K Animals
%K Butterflies/classification/*genetics
%K Genes, Insect
%K Genetic Loci
%K Genetics, Population
%K Genotyping Techniques
%K Geography
%K Likelihood Functions
%K Pigmentation
%K Polymorphism, Single Nucleotide
%K Sequence Analysis, DNA
%K South America
%K Sympatry
%X
The Heliconius butterflies are a diverse recent radiation comprising multiple levels of divergence with ongoing gene flow between species. The recently sequenced genome of Heliconius melpomene allowed us to investigate the genomic evolution of this group using dense RAD marker sequencing. Phylogenetic analysis of 54 individuals robustly supported reciprocal monophyly of H. melpomene and Heliconius cydno and refuted previous phylogenetic hypotheses that H. melpomene may be paraphylectic with respect to H. cydno. Heliconius timareta also formed a monophyletic clade closely related but distinct from H. cydno with Heliconius heurippa falling within this clade. We find evidence for genetic admixture between sympatric populations of the sister clades H. melpomene and H. cydno/timareta, particularly between H. cydno and H. melpomene from Central America and between H. timareta and H. melpomene from the eastern slopes of the Andes. Between races, divergence is primarily explained by isolation by distance and there is no detectable genetic population structure between parapatric races, suggesting that hybrid zones between races are not zones of secondary contact. Our results also support previous findings that colour pattern loci are shared between populations and species with similar colour pattern elements. Furthermore, this pattern is almost unique to these genomic regions, with only a very small number of other loci showing significant similarity between populations and species with similar colour patterns.
%B Molecular Ecology
%V 22
%P 814-826
%8 Feb
%@ 1365-294X (Electronic)0962-1083 (Linking)
%G eng
%M 22924870
%0 Journal Article
%J Philosophical Transactions of the Royal Society B
%D 2012
%T Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing
%A Nadeau, N. J.
%A Whibley, A.
%A Jones, R. T.
%A Davey, J. W.
%A Dasmahapatra, K. K.
%A Baxter, S. W.
%A Quail, M. A.
%A Joron, M.
%A ffrench-Constant, R. H.
%A Blaxter, M. L.
%A Mallet, J.
%A Jiggins, C. D.
%K *Genetic Variation
%K *Genome, Insect
%K *Genomic Islands
%K Adaptation, Biological/genetics
%K Animals
%K Base Sequence
%K Butterflies/classification/*genetics/physiology
%K Chromosomes, Insect/genetics
%K Genes, Insect
%K Genetic Loci
%K Genetic Speciation
%K Genetics, Population
%K Molecular Mimicry
%K Molecular Sequence Data
%K Phylogeny
%K Sequence Analysis, DNA/*methods
%K Species Specificity
%K Wing/physiology
%X
Heliconius butterflies represent a recent radiation of species, in which wing pattern divergence has been implicated in speciation. Several loci that control wing pattern phenotypes have been mapped and two were identified through sequencing. These same gene regions play a role in adaptation across the whole Heliconius radiation. Previous studies of population genetic patterns at these regions have sequenced small amplicons. Here, we use targeted next-generation sequence capture to survey patterns of divergence across these entire regions in divergent geographical races and species of Heliconius. This technique was successful both within and between species for obtaining high coverage of almost all coding regions and sufficient coverage of non-coding regions to perform population genetic analyses. We find major peaks of elevated population differentiation between races across hybrid zones, which indicate regions under strong divergent selection. These 'islands' of divergence appear to be more extensive between closely related species, but there is less clear evidence for such islands between more distantly related species at two further points along the 'speciation continuum'. We also sequence fosmid clones across these regions in different Heliconius melpomene races. We find no major structural rearrangements but many relatively large (greater than 1 kb) insertion/deletion events (including gain/loss of transposable elements) that are variable between races.
%B Philosophical Transactions of the Royal Society B
%V 367
%P 343-53
%8 Feb 5
%@ 1471-2970 (Electronic)0962-8436 (Linking)
%G eng
%M 22201164
%2 3233711
%0 Journal Article
%J Biology Letters
%D 2012
%T Selective bird predation on the peppered moth: the last experiment of Michael Majerus
%A Cook, L. M.
%A Grant, B. S.
%A Saccheri, I. J.
%A Mallet, J.
%K Animals
%K Biological Evolution
%K Birds/*physiology
%K Female
%K Insectivora/physiology
%K Male
%K Melanosis/metabolism
%K Moths/metabolism/*physiology
%K Population Density
%K Predatory Behavior/*physiology
%K Selection, Genetic
%K Species Specificity
%K survival analysis
%X
Colour variation in the peppered moth Biston betularia was long accepted to be under strong natural selection. Melanics were believed to be fitter than pale morphs because of lower predation at daytime resting sites on dark, sooty bark. Melanics became common during the industrial revolution, but since 1970 there has been a rapid reversal, assumed to have been caused by predators selecting against melanics resting on today's less sooty bark. Recently, these classical explanations of melanism were attacked, and there has been general scepticism about birds as selective agents. Experiments and observations were accordingly carried out by Michael Majerus to address perceived weaknesses of earlier work. Unfortunately, he did not live to publish the results, which are analysed and presented here by the authors. Majerus released 4864 moths in his six-year experiment, the largest ever attempted for any similar study. There was strong differential bird predation against melanic peppered moths. Daily selection against melanics (s approximately 0.1) was sufficient in magnitude and direction to explain the recent rapid decline of melanism in post-industrial Britain. These data provide the most direct evidence yet to implicate camouflage and bird predation as the overriding explanation for the rise and fall of melanism in moths.
%B Biology Letters
%V 8
%P 609-612
%8 Aug 23
%@ 1744-957X (Electronic)1744-9561 (Linking)
%G eng
%M 22319093
%2 3391436
%0 Journal Article
%J Pigment Cell and Melanoma Research
%D 2012
%T Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation
%A Kronforst, M. R.
%A Barsh, G. S.
%A Kopp, A.
%A Mallet, J.
%A Monteiro, A.
%A Mullen, S. P.
%A Protas, M.
%A Rosenblum, E. B.
%A Schneider, C. J.
%A Hoekstra, HE
%K *Genetic Variation
%K *Nature
%K Animals
%K Butterflies/anatomy & histology/genetics
%K Melanins/metabolism
%K Pigmentation/*genetics
%K Wing/anatomy & histology
%X
Animals display incredibly diverse color patterns yet little is known about the underlying genetic basis of these phenotypes. However, emerging results are reshaping our view of how the process of phenotypic evolution occurs. Here, we outline recent research from three particularly active areas of investigation: melanin pigmentation in Drosophila, wing patterning in butterflies, and pigment variation in lizards. For each system, we highlight (i) the function and evolution of color variation, (ii) various approaches that have been used to explore the genetic basis of pigment variation, and (iii) conclusions regarding the genetic basis of convergent evolution which have emerged from comparative analyses. Results from these studies indicate that natural variation in pigmentation is a particularly powerful tool to examine the molecular basis of evolution, especially with regard to convergent or parallel evolution. Comparison of these systems also reveals that the molecular basis of convergent evolution is heterogeneous, sometimes involving conserved mechanisms and sometimes not. In the near future, additional work in other emerging systems will substantially expand the scope of available comparisons.
%B Pigment Cell and Melanoma Research
%V 25
%P 411-433
%8 Jul
%@ 1755-148X (Electronic)1755-1471 (Linking)
%G eng
%M 22578174
%0 Journal Article
%J Nature
%D 2011
%T Catfish mimics (News and Views on Alexandrou et al. article in same issue).
%A Mallet, J. & Dasmahapatra, K.
%X
Mutualism can be a double-edged sword if the animals concerned also competefor food. This may explain the discovery that mimic catfish in the Amazon rarelyengage in mimicry with related species.
%B Nature
%V 469
%P 41-42
%G eng
%& 41
%0 Journal Article
%J Insect Conservation and Diversity
%D 2011
%T Hybridisation and climate change: brown argus butterflies in Britain (Polyommatus subgenus Aricia)
%A Mallet, James
%A Wynne, Ian R.
%A Thomas, Chris D.
%B Insect Conservation and Diversity
%V 4
%P 192-199
%@ 1752458X
%G eng
%0 Journal Article
%J Ecological Entomology
%D 2011
%T Selection for enemy-free space: eggs placed away from the host plant increase survival of a neotropical ithomiine butterfly
%A De-Silva, Donna Lisa
%A VÁSquez, Armando Silva
%A Mallet, James
%X
1. The selection of an oviposition site by a phytophagous insect can depend on many factors, including the risk of predation. Many species avoid predators by laying eggs where enemies searching host plants are unlikely to find them. 2. Females of the Peruvian butterfly, Oleria onega Hewitson (Lepidoptera: Nymphalidae: Danainae: Ithomiini) lay most of their eggs (76 ± 9%) off the host plant, Solanum mite Ruiz & Pav. These off-host eggs may be laid up to 0.5 m from the nearest host-plant individual, on twigs or leaf litter, as well as on living plants of species unsuitable for larval food. 3. Disappearance of eggs on and off the host plant was recorded by transferring eggs laid in captivity to known locations in the wild and recording rates of disappearance before the larvae emerged. After 2 days, eggs on the host were significantly more likely to have disappeared compared to eggs laid elsewhere. 4. We conclude that a high risk of predation is a likely trigger that caused O. onega to evolve a behaviour of laying eggs off its host plant.
%B Ecological Entomology
%V 36
%P 667-672
%@ 03076946
%G eng
%0 Journal Article
%J Proceedings of the National Academy of Sciences, USA
%D 2011
%T A wing patterning gene redefines the mimetic history of Heliconius butterflies.
%A Hines, H. M.
%A Counterman, B. A.
%A Papa, R.
%A Albuquerque de Moura P,
%A Cardoso, MZ
%A Linares, M.
%A Mallet J,
%A Reed, R. D.
%A Jiggins, C. D.
%A Kronforst, M. R.
%A McMillan, W. O.
%K Müllerian mimicry | population genetics | phylogeography
%X
The mimetic butterflies Heliconius erato and Heliconius melpomenehave undergone parallel radiations to form a near-identical patchworkof over 20 different wing-pattern races across the Neotropics.Previous molecular phylogenetic work on these radiations has suggestedthat similar but geographically disjunct color patterns arosemultiple times independently in each species. The neutral markersused in these studies, however, can move freely across color patternboundaries, and therefore might not represent the history ofthe adaptive traits as accurately as markers linked to color patterngenes. To assess the evolutionary histories across different loci, wecompared relationships among races within H. erato and within H.melpomene using a series of unlinked genes, genes linked to colorpattern loci, and optix, a gene recently shown to control red colorpatternvariation.We found that although unlinked genes partitionpopulations by geographic region, optix had a different history,structuring lineages by red color patterns and supporting a singleorigin of red-rayed patterns within each species. Genes closelylinked (80–250 kb) to optix exhibited only weak associations withcolor pattern. This study empirically demonstrates the necessity ofexamining phenotype-determining genomic regions to understandthe history of adaptive change in rapidly radiating lineages. Withthese refined relationships, we resolve a long-standing debateabout the origins of the races within each species, supporting thehypothesis that the red-rayed Amazonian pattern evolved recentlyand expanded, causing disjunctions of more ancestral patterns.
%B Proceedings of the National Academy of Sciences, USA
%V 108
%P 19666-19671
%G eng
%0 Journal Article
%J Molecular Ecology
%D 2010
%T The anatomy of a 'suture zone' in Amazonian butterflies: a coalescent-based test for vicariant geographic divergence and speciation
%A Dasmahapatra, K. K.
%A Lamas, G.
%A Simpson, F.
%A Mallet, J.
%K *Genetic Speciation
%K *Genetics, Population
%K Animals
%K Bayes Theorem
%K Butterflies/*genetics
%K Cell Nucleus/genetics
%K coalescent theory
%K DNA, Mitochondrial/genetics
%K Geography
%K Heliconius
%K Ithomiini
%K Likelihood Functions
%K Models, Genetic
%K Molecular Sequence Data
%K Multilocus Sequence Typing
%K Peru
%K phylogeography
%K Pleistocene refuges
%K Population Density
%K Sequence Analysis, DNA
%K Speciation
%X
Attempts by biogeographers to understand biotic diversification in the Amazon have often employed contemporary species distribution patterns to support particular theories, such as Pleistocene rainforest refugia, rather than to test among alternative hypotheses. Suture zones, narrow regions where multiple contact zones and hybrid zones between taxa cluster, have been seen as evidence for past expansion of whole biotas that have undergone allopatric divergence in vicariant refuges. We used coalescent analysis of mutilocus sequence data to examine population split times in 22 pairs of geminate taxa in ithomiine and heliconiine butterflies. We test a hypothesis of simultaneous divergence across a suture zone in NE Peru. Our results reveal a scattered time course of diversification in this suture zone, rather than a tight cluster of split times. Additionally, we find rapid diversification within some lineages such as Melinaea contrasting with older divergence within lineages such as the Oleriina (Hyposcada and Oleria). These results strongly reject simple vicariance as a cause of the suture zone. At the same time, observed lineage effects are incompatible with a series of geographically coincident vicariant events which should affect all lineages similarly. Our results suggest that Pleistocene climatic forcing cannot readily explain this Peruvian suture zone. Lineage-specific biological traits, such as characteristic distances of gene flow or varying rates of parapatric divergence, may be of greater importance.
%B Molecular Ecology
%V 19
%P 4283-4301
%8 Oct
%@ 1365-294X (Electronic)0962-1083 (Linking)
%G eng
%M 20819158
%0 Journal Article
%J Evolution
%D 2010
%T Are species real? The shape of the species boundary with exponential failure, reinforcement, and the "missing snowball"
%A Gourbiere, S.
%A Mallet, J.
%K *Biological Evolution
%K Animals
%K Lepidoptera/*classification/genetics/physiology
%K Models, Theoretical
%K Sexual Behavior, Animal
%K Species Specificity
%X
Under simple assumptions, the evolution of epistatic "Dobzhansky-Muller" incompatibilities between a pair of species should yield an accelerating decline of log overall reproductive compatibility--a "snowball" effect that might rapidly provide new species with "reality." Possible alternatives include: (1) simple exponential failure, giving a linear rate of log compatibility loss, and (2) "slowdown," likely during reinforcement in which mate choice evolves to prevent deleterious hybridization, yielding a decelerating log compatibility loss. In analyses of multiple datasets, we find little support for the snowball effect, except possibly in Lepidoptera hybrid viability. The snowball predicts a slow initial rate of incompatibility acquisition, with low initial variance; instead, highly variable compatibility is almost universally observed at low genetic distances. Another deviation from predictions is that reproductive isolation usually remains incomplete until long after speciation. These results do not disprove snowball compatibility decay, but can result if large deleterious effects are due to relatively few genetic changes, or if different types of incompatibility evolve at very different rates. On the other hand, data on Bacillus and Saccharomyces, as well as theories of chromosomal evolution, suggest that some kinds of incompatibility accumulate approximately linearly, without Dobzhansky-Muller effects. In microorganisms, linearity can result from direct negative effects of DNA sequence divergence on compatibility. Finally, a decelerating slowdown model is supported for sympatric Leptasterias starfish, and in Drosophila prezygotic isolation in sympatry but not allopatry, providing novel comparative evidence for reinforcement.
%B Evolution
%V 64
%P 1-24
%8 Jan
%@ 1558-5646 (Electronic)0014-3820 (Linking)
%G eng
%M 19780810
%0 Journal Article
%J PLoS Genetics
%D 2010
%T Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in Heliconius erato
%A Counterman, B. A.
%A Araujo-Perez, F.
%A Hines, H. M.
%A Baxter, S. W.
%A Morrison, C. M.
%A Lindstrom, D. P.
%A Papa, R.
%A Ferguson, L.
%A Joron, M.
%A ffrench-Constant, R. H.
%A Smith, C. P.
%A Nielsen, D. M.
%A Chen, R.
%A Jiggins, C. D.
%A Reed, R. D.
%A Halder, G.
%A Mallet, J.
%A McMillan, W. O.
%K *Genetics, Population
%K Adaptation, Physiological/*genetics
%K Animals
%K Butterflies/*genetics
%K Chromosomes, Artificial, Bacterial/genetics
%K Gene Expression Regulation
%K Genetic Loci/genetics
%K Genetic Variation
%K Genome/*genetics
%K Genotype
%K Hybridization, Genetic
%K Linkage Disequilibrium/genetics
%K Open Reading Frames/genetics
%K Peru
%K Phenotype
%K Physical Chromosome Mapping
%K Pigmentation/genetics
%K Polymorphism, Single Nucleotide/genetics
%K Sequence Analysis, DNA
%X
Wing pattern evolution in Heliconius butterflies provides some of the most striking examples of adaptation by natural selection. The genes controlling pattern variation are classic examples of Mendelian loci of large effect, where allelic variation causes large and discrete phenotypic changes and is responsible for both convergent and highly divergent wing pattern evolution across the genus. We characterize nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium (LD), and candidate gene expression patterns across two unlinked genomic intervals that control yellow and red wing pattern variation among mimetic forms of Heliconius erato. Despite very strong natural selection on color pattern, we see neither a strong reduction in genetic diversity nor evidence for extended LD across either patterning interval. This observation highlights the extent that recombination can erase the signature of selection in natural populations and is consistent with the hypothesis that either the adaptive radiation or the alleles controlling it are quite old. However, across both patterning intervals we identified SNPs clustered in several coding regions that were strongly associated with color pattern phenotype. Interestingly, coding regions with associated SNPs were widely separated, suggesting that color pattern alleles may be composed of multiple functional sites, conforming to previous descriptions of these loci as "supergenes." Examination of gene expression levels of genes flanking these regions in both H. erato and its co-mimic, H. melpomene, implicate a gene with high sequence similarity to a kinesin as playing a key role in modulating pattern and provides convincing evidence for parallel changes in gene regulation across co-mimetic lineages. The complex genetic architecture at these color pattern loci stands in marked contrast to the single casual mutations often identified in genetic studies of adaptation, but may be more indicative of the type of genetic changes responsible for much of the adaptive variation found in natural populations.
%B PLoS Genetics
%V 6(2)
%P e1000796
%8 Feb
%@ 1553-7404 (Electronic)1553-7390 (Linking)
%G eng
%M 20140239
%2 2816678
%0 Journal Article
%J PLoS Genetics
%D 2010
%T Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in the Heliconius melpomene clade
%A Baxter, S. W.
%A Nadeau, N. J.
%A Maroja, L. S.
%A Wilkinson, P.
%A Counterman, B. A.
%A Dawson, A.
%A Beltran, M.
%A Perez-Espona, S.
%A Chamberlain, N.
%A Ferguson, L.
%A Clark, R.
%A Davidson, C.
%A Glithero, R.
%A Mallet, J.
%A McMillan, W. O.
%A Kronforst, M.
%A Joron, M.
%A ffrench-Constant, R. H.
%A Jiggins, C. D.
%K *Genetics, Population
%K Adaptation, Physiological/*genetics
%K Animals
%K Butterflies/genetics
%K Chromosomes, Artificial, Bacterial/genetics
%K Gene Expression Regulation
%K Genes, Insect/genetics
%K Genetic Loci/genetics
%K Genetic Variation
%K Genome/*genetics
%K Genotype
%K Insect Proteins/genetics/metabolism
%K Linkage Disequilibrium/genetics
%K Molecular Mimicry/*genetics
%K Phenotype
%K Phylogeny
%K Population dynamics
%K Selection, Genetic/genetics
%K Species Specificity
%X
Wing patterning in Heliconius butterflies is a longstanding example of both Mullerian mimicry and phenotypic radiation under strong natural selection. The loci controlling such patterns are "hotspots" for adaptive evolution with great allelic diversity across different species in the genus. We characterise nucleotide variation, genotype-by-phenotype associations, linkage disequilibrium, and candidate gene expression at two loci and across multiple hybrid zones in Heliconius melpomene and relatives. Alleles at HmB control the presence or absence of the red forewing band, while alleles at HmYb control the yellow hindwing bar. Across HmYb two regions, separated by approximately 100 kb, show significant genotype-by-phenotype associations that are replicated across independent hybrid zones. In contrast, at HmB a single peak of association indicates the likely position of functional sites at three genes, encoding a kinesin, a G-protein coupled receptor, and an mRNA splicing factor. At both HmYb and HmB there is evidence for enhanced linkage disequilibrium (LD) between associated sites separated by up to 14 kb, suggesting that multiple sites are under selection. However, there was no evidence for reduced variation or deviations from neutrality that might indicate a recent selective sweep, consistent with these alleles being relatively old. Of the three genes showing an association with the HmB locus, the kinesin shows differences in wing disc expression between races that are replicated in the co-mimic, Heliconius erato, providing striking evidence for parallel changes in gene expression between Mullerian co-mimics. Wing patterning loci in Heliconius melpomene therefore show a haplotype structure maintained by selection, but no evidence for a recent selective sweep. The complex genetic pattern contrasts with the simple genetic basis of many adaptive traits studied previously, but may provide a better model for most adaptation in natural populations that has arisen over millions rather than tens of years.
%B PLoS Genetics
%V 6(2)
%P e1000794
%8 Feb
%@ 1553-7404 (Electronic)1553-7390 (Linking)
%G eng
%M 20140188
%2 2816687
%0 Journal Article
%J Philosophical Transactions of the Royal Society
%D 2010
%T Group selection and the development of the biological species concept
%A Mallet, J.
%K *Genetic Speciation
%K *Models, Genetic
%K *Selection, Genetic
%K Animals
%K Biological Evolution
%K Female
%K Genetics/history
%K History, 19th Century
%K History, 20th Century
%K History, 21st Century
%K Male
%X
The development of what became known as the biological species concept began with a paper by Theodosius Dobzhansky in 1935, and was amplified by a mutualistic interaction between Dobzhansky, Alfred Emerson and Ernst Mayr after the second world war. By the 1950s and early 1960s, these authors had developed an influential concept of species as coadapted genetic complexes at equilibrium. At this time many features of species were seen as group advantages maintained by selection to avoid breakdown of beneficial coadaptation and the 'gene pool'. Speciation thus seemed difficult. It seemed to require, more so than today, an external deus ex machina, such as allopatry or the founder effect, rather than ordinary within-species processes of natural selection, sexual selection, drift and gene flow. In the mid-1960s, the distinctions between group and individual selection were clarified. Dobzhansky and Mayr both understood the implications, but their views on species changed little. These group selectionist ideas now seem peculiar, and are becoming distinctly less popular today. Few vestiges of group selectionism and species-level adaptationism remain in recent reviews of speciation. One wonders how many of our own cherished views on evolution will seem as odd to future biologists.
%B Philosophical Transactions of the Royal Society
%V 365
%P 1853-1863
%8 Jun 12
%@ 1471-2970 (Electronic)0962-8436 (Linking)
%G eng
%M 20439286
%2 2871894
%0 Journal Article
%J Molecular Ecology Resources
%D 2010
%T Mitochondrial DNA barcoding detects some species that are real, and some that are not
%A Dasmahapatra, K. K.
%A Elias, M.
%A Hill, R. I.
%A Hoffman, J. I.
%A Mallet, J.
%X
Mimicry and extensive geographical subspecies polymorphism combine to make species in the ithomiine butterfly genus Mechanitis (Lepidoptera; Nymphalidae) difficult to determine. We use mitochondrial DNA (mtDNA) barcoding, nuclear sequences and amplified fragment length polymorphism (AFLP) genotyping to investigate species limits in this genus. Although earlier biosystematic studies based on morphology described only four species, mtDNA barcoding revealed eight well-differentiated haplogroups, suggesting the presence of four new putative 'cryptic species'. However, AFLP markers supported only one of these four new 'cryptic species' as biologically meaningful. We demonstrate that in this genus, deep genetic divisions expected on the basis of mtDNA barcoding are not always reflected in the nuclear genome, and advocate the use of AFLP markers as a check when mtDNA barcoding gives unexpected results.
%B Molecular Ecology Resources
%V 10
%P 264-273
%8 Mar
%@ 1755-0998 (Electronic)1755-098X (Linking)
%G eng
%M 21565021
%0 Journal Article
%J Molecular Phylogenetics and Evolution
%D 2010
%T Molecular phylogenetics of the neotropical butterfly subtribe Oleriina (Nymphalidae: Danainae: Ithomiini)
%A de-Silva, D. L.
%A Day, J. J.
%A Elias, M.
%A Willmott, K.
%A Whinnett, A.
%A Mallet, J.
%K *Genetic Speciation
%K *Phylogeny
%K Animals
%K Bayes Theorem
%K Butterflies/*classification/genetics
%K Cell Nucleus/genetics
%K DNA, Mitochondrial/genetics
%K Evolution, Molecular
%K Geography
%K Likelihood Functions
%K Models, Genetic
%K Sequence Analysis, DNA
%K South America
%X
The Oleriina is one of the most speciose subtribes of the neotropical nymphalid butterfly tribe Ithomiini. They are widely distributed across the Andes and Amazonian lowlands and like other ithomiines they are involved in complex mimicry rings. This subtribe is of particular interest because it contains the most diverse ithomiine genus, Oleria, as well as two genera, Megoleria and Hyposcada, that feed on hostplants not utilized elsewhere in the tribe. Here we present the first comprehensive species-level phylogeny for the Oleriina, representing 83% of recognised species in the group, and based on 6698bp from eight mitochondrial (mt) and nuclear (nc) genes. Topologies are largely congruent for ncDNA and the concatenated dataset and the genera Oleria, Hyposcada and Megoleria are recovered and well-supported, although strongly discordant genealogy between mtDNA and ncDNA suggest possible introgression among Hyposcada and Megoleria. A fourth clade containing the type species of Ollantaya is consistently recovered, and this recently synonymized name is resurrected. Clear subdivisions within Oleria separate the genus into four species groups, onega, amalda, makrena and aegle, which also correspond to differing biogeographic and elevation range characteristics. Unlike other ithomiine genera, the Oleriina show homogeneity in mimetic wing pattern, in sharp contrast to the emerging paradigm that mimetic shifts have enhanced diversification in the tribe. Our results show a potentially more important role for geographic isolation in the diversification of the Oleriina compared to other Ithomiini studied to date and provide a framework for more detailed biogeographical studies, in addition to a rare opportunity for comparative analyses with other neotropical groups.
%B Molecular Phylogenetics and Evolution
%V 55
%P 1032-1041
%8 Jun
%@ 1095-9513 (Electronic)1055-7903 (Linking)
%G eng
%M 20079859
%0 Journal Article
%J Ecological Entomology
%D 2010
%T Shift happens! Shifting balance and the evolution of diversity in warning colour and mimicry
%A Mallet, James
%B Ecological Entomology
%V 35
%P 90-104
%@ 0307694613652311
%G eng
%N Suppl. 1)
%0 Journal Article
%J Biology and Philosophy
%D 2010
%T Why was Darwin’s view of species rejected by twentieth century biologists?
%A Mallet, James
%B Biology and Philosophy
%V 25
%P 497-527
%@ 0169-38671572-8404
%G eng
%0 Journal Article
%J Science
%D 2009
%T Policy forum: Biodiversity conservation and the Millennium Development Goals
%A Sachs, JD.
%A Baillie, JEM.
%A Sutherland, WJ.
%A Armsworth, PR.
%A Ash, N.
%A Beddington, J.
%A Blackburn, TM.
%A Collen, B.
%A Gardiner, B.
%A Gaston, KJ.
%A Godfray, HCJ.
%A Green, RE.
%A Harvey, PH.
%A House, B.
%A Knapp, S.
%A Kümpel, NF.
%A Macdonald, DW.
%A Mace, GM.
%A Mallet, J.
%A Matthews, A.
%A May, RM.
%A Petchey, O.
%A Purvis, A.
%A Roe, D.
%A Safi, K.
%A Turner, K.
%A Walpole, M.
%A Watson, R.
%A Jones, KE.
%B Science
%V 325
%P 1502-1503
%G eng
%0 Book Section
%B Ecology of Butterflies in Europe
%D 2009
%T Bad species
%A Descimon, H.
%A Mallet, J.
%E J Settele,
%E TG Shreeve,
%E M Konvicka,
%E H Van Dyck
%B Ecology of Butterflies in Europe
%I Cambridge University Press
%C Cambridge
%P 219-249
%G eng
%0 Journal Article
%J Gayana
%D 2009
%T Alfred Russel Wallace and the Darwinian species concept: his paper on the swallowtail butterflies (Papilionidae) of 1865.
%A Mallet, J.
%K History of evolution, Mimicry, Species concepts, Geographic variation, Taxonomic inflation,
%K Island biology, Lepidoptera
%X
Soon after his return from the Malay Archipelago, Alfred Russel Wallace published one of his mostsignificant papers. The paper used butterflies of the family Papilionidae as a model system for testingevolutionary hypotheses, and included a revision of the Papilionidae of the region, as well as thedescription of some 20 new species. Wallace argued that the Papilionidae were the most advancedbutterflies, against some of his colleagues such as Bates and Trimen who had claimed that theNymphalidae were more advanced because of their possession of vestigial forelegs. In a very importantsection, Wallace laid out what is perhaps the clearest Darwinist definition of the differences betweenspecies, geographic subspecies, and local ‘varieties.’ He also discussed the relationship of thesetaxonomic categories to what is now termed ‘reproductive isolation.’ While accepting reproductiveisolation as a cause of species, he rejected it as a definition. Instead, species were recognized as formsthat overlap spatially and lack intermediates. However, this morphological distinctness argument breaksdown for discrete polymorphisms, and Wallace clearly emphasised the conspecificity of non-mimeticmales and female Batesian mimetic morphs in Papilio polytes, and also in P. memnon, on the groundsof reproductive continuity. Finally, Wallace detailed how natural selection explains various forms ofparallel evolution, including mimicry.
%B Gayana
%V 73
%P 35-47
%@ 0717-652X
%G eng
%N suppl. 1
%& 35
%0 Journal Article
%J Ecology Briefs. Informative Bulletin of the Centro Internacional de Ecología Tropical (CIET), Caracas
%D 2009
%T Ask the ecologist: Are genetic barcodes the magic tools we need to achieve a precise estimation of biodiversity in tropical ecosystems? What are the advantages and problems associated with this methodological proposal?
%A Mallet, J.
%B Ecology Briefs. Informative Bulletin of the Centro Internacional de Ecología Tropical (CIET), Caracas
%V 1
%P 3
%G eng
%0 Journal Article
%J Journal of Evolutionary Biology
%D 2009
%T Space, sympatry and speciation
%A Mallet, J.
%A A Meyer
%A Nosil, P.
%A Feder, J. L.
%K *Genetic Speciation
%K *Geography
%K Animals
%K Gene Flow
%K Homing Behavior
%K Population dynamics
%K Selection, Genetic
%K Terminology as Topic
%X
Sympatric speciation remains controversial. 'Sympatry' originally meant "in the same geographical area". Recently, evolutionists have redefined 'sympatric speciation' non-spatially to require panmixia (m = 0.5) between a pair of demes before onset of reproductive isolation. Although panmixia is a suitable starting point in models of speciation, it is not a useful definition of sympatry in natural populations, because it becomes virtually impossible to find or demonstrate sympatry in nature. The newer, non-spatial definition fails to address the classical debate about whether natural selection within a geographic overlap regularly causes speciation in nature, or whether complete geographic isolation is usually required. We therefore propose a more precise spatial definition by incorporating the population genetics of dispersal (or 'cruising range'). Sympatric speciation is considerably more likely under this spatial definition than under the demic definition, because distance itself has a powerful structuring effect, even over small spatial scales comparable to dispersal. Ecological adaptation in two-dimensional space often acts as a 'magic trait' that causes pleiotropic reductions of gene flow. We provide examples from our own research.
%B Journal of Evolutionary Biology
%V 22
%P 2332-2341
%8 Nov
%@ 1420-9101 (Electronic)1010-061X (Linking)
%G eng
%M 19732264
%0 Journal Article
%J Biological Journal of the Linnean Society
%D 2008
%T Mayr's view of Darwin: was Darwin wrong about speciation?
%A Mallet, J.
%B Biological Journal of the Linnean Society
%V 95
%P 3-16
%G eng
%0 Journal Article
%J Philosophical Transactions of the Royal Society B-Biological Sciences
%D 2008
%T Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation
%A Mallet, J.
%K *Biological Evolution
%K *Genetic Speciation
%K *Models, Biological
%K Animals
%K Humans
%K Hybridization, Genetic/*genetics
%K Reproduction/genetics
%K Species Specificity
%X
Species are generally viewed by evolutionists as 'real' distinct entities in nature, making speciation appear difficult. Charles Darwin had originally promoted a very different uniformitarian view that biological species were continuous with 'varieties' below the level of species and became distinguishable from them only when divergent natural selection led to gaps in the distribution of morphology. This Darwinian view on species came under immediate attack, and the consensus among evolutionary biologists today appears to side more with the ideas of Ernst Mayr and Theodosius Dobzhansky, who argued 70 years ago that Darwin was wrong about species. Here, I show how recent genetic studies of supposedly well-behaved animals, such as insects and vertebrates, including our own species, have supported the existence of the Darwinian continuum between varieties and species. Below the level of species, there are well-defined ecological races, while above the level of species, hybridization still occurs, and may often lead to introgression and, sometimes, hybrid speciation. This continuum is evident, not only across vast geographical regions, but also locally in sympatry. The existence of this continuum provides good evidence for gradual evolution of species from ecological races and biotypes, to hybridizing species and, ultimately, to species that no longer cross. Continuity between varieties and species not only provides an excellent argument against creationism, but also gives insight into the process of speciation. The lack of a hiatus between species and ecological races suggests that speciation may occur, perhaps frequently, in sympatry, and the abundant intermediate stages suggest that it is happening all around us. Speciation is easy!
%B Philosophical Transactions of the Royal Society B-Biological Sciences
%V 363
%P 2971-2986
%8 Sep 27
%@ 1471-2970 (Electronic)0962-8436 (Linking)
%G eng
%M 18579473
%2 2607318
%0 Journal Article
%J Journal of Insect Science
%D 2007
%T Conserved but flexible: Genetic control of mimicry in Heliconius butterfly wing patterns
%A Joron, Mathieu
%A Papa, Riccardo
%A Mallet, James
%A McMillan, W. Owen
%A Jiggins, Chris D.
%X It is now well known that convergent morphology can evolve via repeated recruitment of the same regulatory genes in different lineages. We here contrast three butterfly species, all classic examples of Müllerian mimicry. We use a genetic linkage map to show that a locus, Yb, controlling the presence of a yellow band in geographic races of H. melpomene maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a ’supergene’ determining multiple, sympatric morphs in a third species, H. numata, a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Hence, a single locus from the multilocus colour pattern architecture in H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic ’supergene’ polymorphism without intermediates. Our results imply that a conserved, yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions. In: Meeting Abstracts: 7th International Workshop on the Molecular Biology and Genetics of the Lepidoptera, August 20–26, 2006, Orthodox Academy of Crete, Kolympari, Crete, Greece
%B Journal of Insect Science
%V 7
%P 24
%G eng
%U https://doi.org/10.1673/031.007.2901
%N 1:29
%0 Journal Article
%J Bulletin of Entomological Research
%D 2007
%T Temporal and spatial incidence of alleles conferring knockdown resistance to pyrethroids in the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae), and their association with other insecticide resistance mechanisms
%A Anstead, JA.
%A Mallet, J.
%A Denholm, I.
%B Bulletin of Entomological Research
%V 97
%P 243-252
%G eng
%0 Journal Article
%J Biological Journal of the Linnean Society
%D 2007
%T Do pollen feeding and pupal-mating have a single origin in Heliconius? Inferences from multilocus sequence data.
%A Beltrán, M.
%A Jiggins, CD.
%A Brower, AVZ.
%A Bermingham, E.
%A Mallet, J.
%K Bayesian analysis – Ef1a – mimicry – mtDNA – parsimony – phylogeny.
%X
%B Biological Journal of the Linnean Society
%V 92
%P 221-239
%G eng
%& 221
%0 Journal Article
%J Biology Letters
%D 2007
%T Genetic analysis of a wild-caught hybrid between non-sister Heliconius butterfly species
%A Dasmahapatra, K. K.
%A Silva-Vasquez, A.
%A Chung, J. W.
%A Mallet, J.
%K *Hybridization, Genetic
%K Animals
%K Butterflies/anatomy & histology/classification/*genetics
%K Female
%K Genetic Markers
%K Inbreeding
%K Male
%K Phylogeny
%K Sequence Analysis, DNA
%X
Interspecific hybridization occurs regularly in wild Heliconius butterflies, although hybrid individuals are usually very rare. However, hybridization generally occurs only between the most closely related species. We report a rare naturally occurring hybrid between non-sister species and carry out the first genetic analysis of such distant hybridization. Mitochondrial and nuclear genes indicate that the specimen is an F1 hybrid between a female Heliconius ethilla and a male Heliconius melpomene, originating from a group of 13 species estimated to have diverged over 2.5 Myr ago. The presence of such distant natural hybrids, together with evidence for backcrossing, suggests that gene flow across species boundaries can take place long after speciation. Adaptive genes such as those involved in wing coloration could thus be widely shared among members of this highly mimetic genus.
Botanists have long believed that hybrid speciation is important, especially after chromosomal doubling (allopolyploidy). Until recently, hybridization was not thought to play a very constructive part in animal evolution. Now, new genetic evidence suggests that hybrid speciation, even without polyploidy, is more common in plants and also animals than we thought.
%B Nature
%V 446
%P 279-283
%8 Mar 15
%@ 1476-4687 (Electronic)0028-0836 (Linking)
%G eng
%M 17361174
%0 Journal Article
%J Proceedings of the Royal Society
%D 2007
%T Limited performance of DNA barcoding in a diverse community of tropical butterflies
%A Elias, M.
%A Hill, R. I.
%A Willmott, K. R.
%A Dasmahapatra, K. K.
%A Brower, A. V.
%A Mallet, J.
%A Jiggins, C. D.
%K Animals
%K Butterflies/*classification/genetics
%K Cluster Analysis
%K DNA, Mitochondrial/chemistry
%K Phylogeny
%K Sequence Analysis, DNA/*methods
%K Tropical Climate
%X
DNA 'barcoding' relies on a short fragment of mitochondrial DNA to infer identification of specimens. The method depends on genetic diversity being markedly lower within than between species. Closely related species are most likely to share genetic variation in communities where speciation rates are rapid and effective population sizes are large, such that coalescence times are long. We assessed the applicability of DNA barcoding (here the 5' half of the cytochrome c oxidase I) to a diverse community of butterflies from the upper Amazon, using a group with a well-established morphological taxonomy to serve as a reference. Only 77% of species could be accurately identified using the barcode data, a figure that dropped to 68% in species represented in the analyses by more than one geographical race and at least one congener. The use of additional mitochondrial sequence data hardly improved species identification, while a fragment of a nuclear gene resolved issues in some of the problematic species. We acknowledge the utility of barcodes when morphological characters are ambiguous or unknown, but we also recommend the addition of nuclear sequence data, and caution that species-level identification rates might be lower in the most diverse habitats of our planet.
%B Proceedings of the Royal Society
%V 274
%P 2881-9
%8 Nov 22
%@ 0962-8452 (Print)0962-8452 (Linking)
%G eng
%M 17785265
%2 3227132
%0 Journal Article
%J BMC Evolutionary Biology
%D 2007
%T Natural hybridization in heliconiine butterflies: the species boundary as a continuum
%A Mallet, J.
%A Beltran, M.
%A Neukirchen, W.
%A Linares, M.
%K *Genetic Speciation
%K *Hybridization, Genetic
%K *Phylogeny
%K Animals
%K Butterflies/classification/*genetics
%K DNA, Mitochondrial/genetics
%K Genetic Markers
%K Genetics, Population
%K Species Specificity
%X
BACKGROUND: To understand speciation and the maintenance of taxa as separate entities, we need information about natural hybridization and gene flow among species. RESULTS: Interspecific hybrids occur regularly in Heliconius and Eueides (Lepidoptera: Nymphalidae) in the wild: 26-29% of the species of Heliconiina are involved, depending on species concept employed. Hybridization is, however, rare on a per-individual basis. For one well-studied case of species hybridizing in parapatric contact (Heliconius erato and H. himera), phenotypically detectable hybrids form around 10% of the population, but for species in sympatry hybrids usually form less than 0.05% of individuals. There is a roughly exponential decline with genetic distance in the numbers of natural hybrids in collections, both between and within species, suggesting a simple "exponential failure law" of compatibility as found in some prokaryotes. CONCLUSION: Hybridization between species of Heliconius appears to be a natural phenomenon; there is no evidence that it has been enhanced by recent human habitat disturbance. In some well-studied cases, backcrossing occurs in the field and fertile backcrosses have been verified in insectaries, which indicates that introgression is likely, and recent molecular work shows that alleles at some but not all loci are exchanged between pairs of sympatric, hybridizing species. Molecular clock dating suggests that gene exchange may continue for more than 3 million years after speciation. In addition, one species, H. heurippa, appears to have formed as a result of hybrid speciation. Introgression may often contribute to adaptive evolution as well as sometimes to speciation itself, via hybrid speciation. Geographic races and species that coexist in sympatry therefore form part of a continuum in terms of hybridization rates or probability of gene flow. This finding concurs with the view that processes leading to speciation are continuous, rather than sudden, and that they are the same as those operating within species, rather than requiring special punctuated effects or complete allopatry. Although not qualitatively distinct from geographic races, nor "real" in terms of phylogenetic species concepts or the biological species concept, hybridizing species of Heliconius are stably distinct in sympatry, and remain useful groups for predicting morphological, ecological, behavioural and genetic characteristics.
%B BMC Evolutionary Biology
%V 7
%P 28
%@ 1471-2148 (Electronic)1471-2148 (Linking)
%G eng
%U http://www.ucl.ac.uk/taxome/hyb/
%M 17319954
%2 1821009
%0 Journal Article
%J PLoS Biology
%D 2006
%T A conserved supergene locus controls colour pattern diversity in Heliconius butterflies
%A Joron, M.
%A Papa, R.
%A Beltran, M.
%A Chamberlain, N.
%A Mavarez, J.
%A Baxter, S.
%A Abanto, M.
%A Bermingham, E.
%A Humphray, S. J.
%A Rogers, J.
%A Beasley, H.
%A Barlow, K.
%A ffrench-Constant, R. H.
%A Mallet, J.
%A McMillan, W. O.
%A Jiggins, C. D.
%K *Biology
%K *Body Patterning
%K *Models, Biological
%K Animals
%K Biodiversity
%K Butterflies/*physiology
%K Chromosomes, Artificial, Bacterial
%K Conserved Sequence
%K Crosses, Genetic
%K Female
%K Male
%K Microsatellite Repeats
%K Models, Genetic
%K Molecular Sequence Data
%K Phenotype
%X
We studied whether similar developmental genetic mechanisms are involved in both convergent and divergent evolution. Mimetic insects are known for their diversity of patterns as well as their remarkable evolutionary convergence, and they have played an important role in controversies over the respective roles of selection and constraints in adaptive evolution. Here we contrast three butterfly species, all classic examples of Mullerian mimicry. We used a genetic linkage map to show that a locus, Yb, which controls the presence of a yellow band in geographic races of Heliconius melpomene, maps precisely to the same location as the locus Cr, which has very similar phenotypic effects in its co-mimic H. erato. Furthermore, the same genomic location acts as a "supergene", determining multiple sympatric morphs in a third species, H. numata. H. numata is a species with a very different phenotypic appearance, whose many forms mimic different unrelated ithomiine butterflies in the genus Melinaea. Other unlinked colour pattern loci map to a homologous linkage group in the co-mimics H. melpomene and H. erato, but they are not involved in mimetic polymorphism in H. numata. Hence, a single region from the multilocus colour pattern architecture of H. melpomene and H. erato appears to have gained control of the entire wing-pattern variability in H. numata, presumably as a result of selection for mimetic "supergene" polymorphism without intermediates. Although we cannot at this stage confirm the homology of the loci segregating in the three species, our results imply that a conserved yet relatively unconstrained mechanism underlying pattern switching can affect mimicry in radically different ways. We also show that adaptive evolution, both convergent and diversifying, can occur by the repeated involvement of the same genomic regions.
%B PLoS Biology
%V 4
%P e303
%8 Oct
%@ 1545-7885 (Electronic)1544-9173 (Linking)
%G eng
%M 17002517
%2 1570757
%0 Journal Article
%J Heredity
%D 2006
%T DNA barcodes: recent successes and future prospects
%A Dasmahapatra, K. K.
%A Mallet, J.
%K Classification
%K DNA, Mitochondrial/*genetics
%K Genetic Techniques/trends
%K Species Specificity
%B Heredity
%V 97
%P 254-255
%8 Oct
%@ 0018-067X (Print)0018-067X (Linking)
%G eng
%M 16788705
%0 Journal Article
%J BMC Biology
%D 2006
%T Polyphyly and gene flow between non-sibling Heliconius species
%A Bull, V.
%A Beltran, M.
%A Jiggins, C. D.
%A McMillan, W. O.
%A Bermingham, E.
%A Mallet, J.
%K *Models, Genetic
%K Animals
%K Biological Evolution
%K Butterflies/*genetics
%K DNA-Binding Proteins/genetics
%K Dopa Decarboxylase/genetics
%K Drosophila Proteins/genetics
%K Electron Transport Complex IV/genetics
%K Gene Flow
%K Haplotypes
%K Introns
%K Mannose-6-Phosphate Isomerase/genetics
%K Phylogeny
%K Species Specificity
%K Transcription Factors/genetics
%K Triose-Phosphate Isomerase/genetics
%X
BACKGROUND: The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America. RESULTS: In these taxa, we sequenced 30-45 haplotypes per locus of a mitochondrial region containing the genes for cytochrome oxidase subunits I and II (CoI/CoII), and intron-spanning fragments of three unlinked nuclear loci: triose-phosphate isomerase (Tpi), mannose-6-phosphate isomerase (Mpi) and cubitus interruptus (Ci) genes. A fifth gene, dopa decarboxylase (Ddc) produced sequence data likely to be from different duplicate loci in some of the taxa, and so was excluded. Mitochondrial and Tpi genealogies are consistent with reciprocal monophyly, whereas sympatric populations of the species in Panama share identical or similar Mpi and Ci haplotypes, giving rise to genealogical polyphyly at the species level despite evidence for rapid sequence divergence at these genes between geographic races of H. melpomene. CONCLUSION: Recent transfer of Mpi haplotypes between species is strongly supported, but there is no evidence for introgression at the other three loci. Our results demonstrate that the boundaries between animal species can remain selectively porous to gene flow long after speciation, and that introgression, even between non-sibling species, can be an important factor in animal evolution. Interspecific gene flow is demonstrated here for the first time in Heliconius and may provide a route for the transfer of switch-gene adaptations for Mullerian mimicry. The results also forcefully demonstrate how reliance on a single locus may give an erroneous picture of the overall genealogical history of speciation and gene flow.
%B BMC Biology
%V 4
%P 11
%@ 1741-7007 (Electronic)1741-7007 (Linking)
%G eng
%M 16630334
%2 1481601
%0 Journal Article
%J Trends in Ecology and Evolution
%D 2006
%T What does Drosophila genetics tell us about speciation?
%A Mallet, J.
%K *Genetic Speciation
%K Animals
%K Butterflies/genetics
%K Cell Differentiation
%K Cell Survival
%K Chimera/genetics
%K Comprehension
%K Drosophila/*genetics
%K Evolution, Molecular
%K Infertility
%K Selection, Genetic
%K Sexual Behavior, Animal
%X
Studies of hybrid inviability, sterility and 'speciation genes' in Drosophila have given insight into the genetic changes that result in reproductive isolation. Here, I survey some extraordinary and important advances in Drosophila speciation research. However, 'reproductive isolation' is not the same as 'speciation', and this Drosophila work has resulted in a lopsided view of speciation. In particular, Drosophila are not always well-suited to investigating ecological and other selection-driven primary causes of speciation in nature. Recent advances have made use of far less tractable, but more charismatic organisms, such as flowering plants, vertebrates and larger insects. Work with these organisms has complemented Drosophila studies of hybrid unfitness to provide a more complete understanding of speciation.
%B Trends in Ecology and Evolution
%V 21
%P 386-93
%8 Jul
%@ 0169-5347 (Print)0169-5347 (Linking)
%G eng
%M 16765478
%0 Journal Article
%J Bulletin of Zoological Nomenclature
%D 2005
%T Case 3320. Papilio sapho Drury, 1782 (currently Heliconius sapho; Insecta, Lepidoptera): proposed conservation of the specific name
%A Lamas, G.
%A Mallet, JLB.
%B Bulletin of Zoological Nomenclature
%V 62
%P 21-24
%G eng
%& 21
%0 Journal Article
%J Journal of Evolutionary Biology
%D 2005
%T Has adaptive dynamics contributed to the understanding of adaptive and sympatric speciation?
%A Gourbiere, S.
%A Mallet, J.
%K *Biological Evolution
%K *Genetics, Population
%K *Models, Theoretical
%K *Population Dynamics
%K Adaptation, Biological/*genetics
%K Mutation/genetics
%K Phenotype
%K Selection, Genetic
%K Species Specificity
%B Journal of Evolutionary Biology
%V 18
%P 1201-1204
%8 Sep
%@ 1010-061X (Print)1010-061X (Linking)
%G eng
%M 16135114
%0 Journal Article
%J Trends in Ecology and Evolution
%D 2005
%T Hybridization as an invasion of the genome
%A Mallet, J.
%X
Hybridization between species is commonplace in plants, but is often seen as unnatural and unusual in animals. Here, I survey studies of natural interspecific hybridization in plants and a variety of animals. At least 25% of plant species and 10% of animal species, mostly the youngest species, are involved in hybridization and potential introgression with other species. Species in nature are often incompletely isolated for millions of years after their formation. Therefore, much evolution of eventual reproductive isolation can occur while nascent species are in gene-flow contact, in sympatry or parapatry, long after divergence begins. Although the relative importance of geographic isolation and gene flow in the origin of species is still unknown, many key processes involved in speciation, such as 'reinforcement' of post-mating isolation by the evolution of assortative mating, will have ample opportunity to occur in the presence of continuing gene flow. Today, DNA sequence data and other molecular methods are beginning to show that limited invasions of the genome are widespread, with potentially important consequences in evolutionary biology, speciation, biodiversity, and conservation.
%B Trends in Ecology and Evolution
%V 20
%P 229-237
%8 May
%@ 0169-5347 (Print)0169-5347 (Linking)
%G eng
%M 16701374
%0 Journal Article
%J European Journal of Entomology
%D 2005
%T Mitochondrial DNA provides an insight into the mechanisms driving diversification in the ithomiine butterfly Hyposcada anchiala (Lepidoptera: Nymphalidae, Ithomiinae)
%A Whinnett, A.
%A Willmott, KR.
%A Brower, AVZ.
%A Simpson, F.
%A Lamas, G.
%A Mallet, J.
%K Mitochondrial DNA, Andes, diversification, Ithomiinae, Hyposcada, mimicry, refuge hypothesis
%X
Geographic subspecies of several ithomiine butterflies on the lower east Andean slopes display a black and orange“melanic tiger” aposematic wing pattern that occurs from Colombia to Bolivia, while geographically adjacent lowland subspeciestypically bear a coloured, “tiger” pattern. However, it is not clear whether subspecies with similar wing patterns in different regionshave arisen through independent events of convergent adaptation, possibly through parapatric differentiation, or result from allopatricdifferentiation, as proposed by the refuge hypothesis. Here, we examine geographic patterns of divergence in the widespreadand common ithomiine butterfly Hyposcada anchiala. We present phylogenetic hypotheses for 5 subspecies of H. anchiala, basedon 1567 bp mitochondrial DNA. All topologies indicated that a single switch in mimetic pattern best explained the wing patterningof the H. anchiala studied here. This finding suggests that the subspecies of H. anchiala studied here result from at least two stagesof differentiation, and is consistent with a single colonisation into a novel altitudinal zone coincident with a wing pattern switch, followedby subsequent divergence within, rather than across altitudinal zones. The subspecies divergences indicated diversificationswere consistent with the Pleistocene. Furthermore, the lowland subspecies were more recently derived than the montane taxa, in contrastto predictions of the “Andean species pump” hypothesis.
%B European Journal of Entomology
%V 102
%P 633-639
%G eng
%& 633
%0 Journal Article
%J Proceedings of the Royal Society B
%D 2005
%T Molecular and behavioural evidence for gene flow between host races of the larch budmoth Zeiraphera diniana (Lepidoptera: Tortricidae)
%A Drès, M.
%A Mallet, J.
%K biotypes, gene flow, host races, hybridization, mitochondrial DNA, introgression, mate
%K choice
%X
Larch and pine associated populations of Zeiraphera diniana (Lepidoptera: Tortricidae) differin a number of heritable traits, but pheromone-mediated cross-attraction occurs betweenthem in the wild. Using a quartet mate choice design (one male and one female of each typeper cage) we estimate that, following cross-attraction by pheromones, the subsequentprobability of hybridization is approximately 28%. We also examined molecular data, andwere unable to distinguish between the races on the basis of 695bp of mitochondrial COI,tRNA-leucine, and COII gene sequence. Both results support earlier field studies suggestingthat larch- and pine-feeding populations are host races that hybridize at an appreciable levelin the wild. The shared mitochondrial haplotypes we observed are also consistent withongoing and successful gene flow between the two host races.
%B Proceedings of the Royal Society B
%V Submitted
%G eng
%0 Journal Article
%J Annals of the Entomological Society of America
%D 2005
%T Phylogenetic utility of Tektin, a novel region for inferring systematic relationships among Lepidoptera
%A Whinnett, A.
%A Brower, AVZ.
%A Lee, M-M.
%A Willmott, KR.
%A Mallet, J.
%K Ithomiinae, Lepidoptera, molecular phylogenetics, Tektin
%X
Rapidly evolving nuclear coding sequences are highly desirable for phylogeneticstudies of closely related species. Here, we investigated an 807-bp region, homologous to the testisspeciÞcTektin gene from Bombyx mori (L.), in 34 nymphalid butterßy taxa in the subfamiliesIthomiinae, Danainae, and Heliconiinae. Within Ithomiinae, relationships inferred from Tektin sequencedata were remarkably similar to those in trees based on combined morphological andecological data. Partitioned Bremer analysis, with mitochondrial cytochrome oxidase I and II, andnuclear wingless and elongation factor 1- sequences, revealed Tektin to have the greatest utility forinferring relationships at the genus, tribe, and subfamily levels across the studied taxa.Wethink Tektinwill provide a useful source of molecular characters for inference of relationships among otherbutterßies, and perhaps among other insect taxa.
%B Annals of the Entomological Society of America
%V 98
%P 873-886
%G eng
%& 873
%0 Journal Article
%J Trends in Ecology and Evolution
%D 2005
%T Response to Harris and Froufe, and Knapp : Taxonomic inflation
%A Mallet, J.
%A Isaac, N.
%A Mace, G.
%B Trends in Ecology and Evolution
%V 20
%P 8-9
%@ 01695347
%G eng
%0 Journal Article
%J Heredity
%D 2005
%T Speciation in the 21st Century. Review of "Speciation", by Jerry A. Coyne & H. Allen Orr
%A Mallet, J.
%B Heredity
%V 95
%P 105-109
%@ 0018-067X1365-2540
%G eng
%0 Journal Article
%J Proceedings of the Royal Society B
%D 2005
%T Strikingly variable divergence times inferred across an Amazonian butterfly 'suture zone'
%A Whinnett, A.
%A Zimmermann, M.
%A Willmott, K. R.
%A Herrera, N.
%A Mallarino, R.
%A Simpson, F.
%A Joron, M.
%A Lamas, G.
%A Mallet, J.
%K *Evolution, Molecular
%K *Genetic Variation
%K *Hybridization, Genetic
%K *Phylogeny
%K Animals
%K Base Sequence
%K Bayes Theorem
%K Butterflies/*genetics
%K DNA Primers
%K DNA, Mitochondrial/genetics
%K Geography
%K Likelihood Functions
%K Models, Genetic
%K Molecular Sequence Data
%K Peru
%K Population dynamics
%K Sequence Analysis, DNA
%K Species Specificity
%X
'Suture zones' are areas where hybrid and contact zones of multiple taxa are clustered. Such zones have been regarded as strong evidence for allopatric divergence by proponents of the Pleistocene forest refugia theory, a vicariance hypothesis frequently used to explain diversification in the Amazon basin. A central prediction of the refugia and other vicariance theories is that the taxa should have a common history so that divergence times should be coincident among taxa. A suture zone for Ithomiinae butterflies near Tarapoto, NE Peru, was therefore studied to examine divergence times of taxa in contact across the zone. We sequenced 1619bp of the mitochondrial COI/COII region in 172 individuals of 31 species from across the suture zone. Inferred divergence times differed remarkably, with divergence between some pairs of widespread species (each of which may have two or more subspecies interacting in the zone, as in the genus Melinaea) being considerably less than that between hybridizing subspecies in other genera (for instance in Oleria). Our data therefore strongly refute a simple hypothesis of simultaneous vicariance and suggest that ongoing parapatric or other modes of differentiation in continuous forest may be important in driving diversification in Amazonia.
%B Proceedings of the Royal Society B
%V 272
%P 2525-2533
%8 Dec 7
%@ 0962-8452 (Print)0962-8452 (Linking)
%G eng
%M 16271979
%2 1599783