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2020
Rosser, N., Shirai, L. T., Dasmahapatra, K. K., Mallet, J., & Freitas, A. V. L. (2020). The Amazon river is a suture zone for a polyphyletic group of co-mimetic heliconiine butterflies. Ecography , 43, 10.1111/ecog.05282. Publisher's Version
OPEN ACCESS
Mallet, J. (2020). Alternative views of biological species: reproductively isolated units or genotypic clusters? National Science Review , 8 (7), 1401-1407. Publisher's VersionAbstract

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.

OPEN ACCESS
Gauthier, J., de Silva, D. L., Gompert, Z., Whibley, A., Houssin, C., Le Poul, Y., McClure, M., et al. (2020). Contrasting genomic and phenotypic outcomes of hybridization between pairs of mimetic butterfly taxa across a suture zone. Molecular Ecology , 29 (7), 1328-1343. Publisher's Version
Qiao, L., Yan, Z. -wen, Xiong, G., Hao, Y. -jin, Wang, R. -xin, Hu, H., Song, J. -bo, et al. (2020). Excess melanin precursors rescue defective cuticular traits in stony mutant silkworms probably by upregulating four genes encoding RR1-type larval cuticular proteins. Insect Biochemistry and Molecular Biology , 119, 103315. Publisher's VersionAbstract
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.
qiao_et_al._2020
Gillespie, R. G., Bennett, G. M., De Meester, L., Feder, J. L., Fleischer, R. C., Harmon, L. J., Hendry, A. P., et al. (2020). Comparing adaptive radiations across space, time, and taxa. Journal of Heredity , 111 (1), 1-20. Publisher's VersionAbstract
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
OPEN ACCESS
2019
Edelman, N. B., Frandsen, P. B., Miyagi, M., Clavijo, B., Davey, J., Dikow, R. B., García-Accinelli, G., et al. (2019). Genomic architecture and introgression shape a butterfly radiation. Science , 366 (November 1), 594-599. Publisher's VersionAbstract

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.

Mallet, J. (2019). Reply to Andrew Brower’s critique of the evidence for hybridization among Heliconius butterfly species in the wild. Zootaxa , 4679, 577-595. Publisher's VersionAbstract
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
OPEN ACCESS
Rosser, N., Queste, L. M., Cama, B., Edelman, N. B., Mann, F., Mori Pezo, R., Morris, J., et al. (2019). Geographic contrasts between pre‐ and postzygotic barriers are consistent with reinforcement in Heliconius butterflies. Evolution , 73 (9), 1821-1838. Publisher's VersionAbstract
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
OPEN ACCESS
Chazot, N., Willmott, K. R., Lamas, G., Freitas, A. V. L., Piron-Prunier, F., Arias, C. F., Mallet, J., et al. (2019). Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation. Global Ecology and Biogeography , 28 (8), 1118–1132. Publisher's VersionAbstract

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.

Ray, D. A., Grimshaw, J. R., Halsey, M. K., Korstian, J. M., Osmanski, A. B., Sullivan, K. A., Wolf, K. A., et al. (2019). Simultaneous TE analysis of 19 heliconiine butterflies yields novel insights into rapid TE-based genome diversification and multiple SINE births and deaths. Genome Biology and Evolution , 11 (8), 2162-2177. Publisher's VersionAbstract
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
OPEN ACCESS
Morris, J., Navarro, N., Rastas, P., Rawlins, L. D., Sammy, J., Mallet, J., & Dasmahapatra, K. K. (2019). The genetic architecture of adaptation: convergence and pleiotropy in Heliconius wing pattern evolution. Heredity , 123, 138-152. Publisher's Version
OPEN ACCESS
Rosser, N., Freitas, A. V. L., Huertas, B., Joron, M., Lamas, G., Mérot, C., Simpson, F., et al. (2019). Cryptic speciation associated with geographic and ecological divergence in two Amazonian Heliconius butterflies. Zoological Journal of the Linnean Society , 186 (1), 233-249. Publisher's VersionAbstract

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.

OPEN ACCESS
2018
Mallet, J., Ehrlich, P., Gill, F. B., McCormack, J., Raven, P., Chan, S., & Goho, S. A. (2018). 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). mallet_et_al._2018_comments_on_esa.pdf
Jay, P., Whibley, A., Frézal, L., de Cara, M. Á. R., Nowell, R. W., Mallet, J., Dasmahapatra, K. D., et al. (2018). Supergene evolution triggered by the introgression of a chromosomal inversion. Current Biology , 28, 1839-1845. Publisher's VersionAbstract
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.
jay_et_al_2018_par-num_inversion.pdf
Mallet, J. (2018). Invasive insect hybridizes with local pests. Proceedings of the National Academy of Sciences , 115 (19), 4819-4821. Published version
Chazot, N., de Silva, D. L., Willmott, K. R., Freitas, A. V. L., Lamas, G., Mallet, J., Giraldo, C. E., et al. (2018). Contrasting patterns of Andean diversification among three diverse clades of Neotropical clearwing butterflies. Ecology and Evolution , 8 (8), 3965-3982. Publisher's Version
OPEN ACCESS
2017
Mallet, J. (2017). Review of: "The Ecology and Evolution of Heliconius Butterflies," by Chris D. Jiggins (2016). Tropical Lepidoptera Research , 27 (2), 120. mallet_2017_jiggins_book_review.pdf
OPEN ACCESS
Van Belleghem, S. M., Rastas, P., Papanicolaou, A., Martin, S. H., Arias, C. F., Supple, M. A., Hanly, J. J., et al. (2017). Complex modular architecture around a simple toolkit of wing pattern genes. Nature Ecology and Evolution , 1 0052. Publisher's Version SUPPLEMENT
de Silva, D. L., Mota, L. L., Chazot, N., Mallarino, R., Silva-Brandão, K. L., Gómez Piñerez, L. M., Freitas, A. V. L., et al. (2017). North Andean origin and diversification of the largest ithomiine butterfly genus [Pteronymia]. Scientific Reports , 7 45966. Publisher's VersionAbstract

 

Article | OPEN

North Andean origin and diversification of the largest ithomiine butterfly genus
  • Donna Lisa De-Silva
  • , Luísa L. Mota
  • , Nicolas Chazot
  • , Ricardo Mallarino
  • , Karina L. Silva-Brandão
  • , Luz Miryam Gómez Piñerez
  • , André V.L. Freitas
  • , Gerardo Lamas
  • , Mathieu Joron
  • , James Mallet
  • , Carlos E. Giraldo
  • , Sandra Uribe
  • , Tiina Särkinen
  • , Sandra Knapp
  • , Chris D. Jiggins
  • , Keith R. Willmott
  •  & Marianne Elias
  • Scientific Reports 7, Article number: 45966 (2017)
  • doi:10.1038/srep45966
  • Download Citation
    • Evolutionary ecology
    • Phylogenetics
Received:
31 October 2016
Accepted:
22 February 2017
Published online:
07 April 2017

Abstract

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 genus Pteronymia (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, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated 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 to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others

OPEN ACCESS
2016
Chazot, N., Willmott, K. R., Condamine, F. L., de Silva, D. L., Freitas, A. V. L., Morlon, H., Giraldo, C. E., et al. (2016). Into the Andes: multiple independent colonizations drive montane diversity in the Neotropical clearwing butterflies Godyridina. Molecular Ecology , 25 (22), 5765-5784. Publisher's VersionAbstract

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.

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Science cover, Nov. 1, 2019
Cover of Science, Nov. 1, 2019.
The issue features our paper on genomic evidence for gene flow among species.  Photo by Andrew Neild.

 

Heliconius demeter vs. eratosignis
A cryptic species discovered in Heliconius !  It is not always the case that mtDNA 'barcode' differences correctly delimit separate species. However, we recently found two cryptic Heliconius species that co-occur in sympatry in a narrow zone of overlap in Amazonia, initially via barcoding. Furthermore, the two taxa are co-mimics, so no mimicry switch led to speciation here, although we had thought that mimicry switches typically accompanied speciation in the genus Heliconius. Rosser et al. 2019.  

 

moving clines

What prevents hybrid zones from moving? (a), top above. Could be there's a density trough (b), or a cline at another ecologically relevant locus that interferes (c)? We argue that it's more likely that a high rainfall peak (d), bottom at the edge of the Andes traps butterfly hybrid zones, to form a massive suture zone in many butterfly taxa. (See Rosser et al. 2014).

 

from Heliconius Nature 2012 Fig. 4

Evidence for adaptive introgression at the B/D mimicry locus
a, Genetic divergence between H. melpomene races aglaope (rayed) and amaryllis (postman) across a hybrid zone in northeast Peru. Divergence, FST, measured along the B/D genomic region peaks in the locus that controls red wing pattern elements between the genes kinesin and optix. b, c, Distribution of fixed ABBA and BABA sites (see above) along B/Dregion for two comparisons between H. melpomene and H. timareta. Excesses of ABBA in b and BABA in care highly significant, indicating introgression of colour pattern control region. From Fig. 4 of Heliconius Genome Consortium 2012


Selection against melanism in UK after the Clean Air Act. Survival of peppered moth morphs (+/- SE) over the course of six years of the predation experiment. Unfilled diamonds with dashed lines, non-melanic; filled squares with solid lines, melanic. From Fig. 1 of Laurence Cook et al. 2012

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