Papers

2016
Mallet, J., Besansky, N., & Hahn, M. W. (2016). How reticulated are species? BioEssays , 38 (2), 140-149.Abstract
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.
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(Open Access)

de Silva, D. L., Elias, M., Willmott, K., Mallet, J., & Day, J. J. (2016). Diversification of clearwing butterflies with the rise of the Andes. Journal of Biogeography , 43, 44-58.Abstract

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.

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(Open Access) doi: 10.1111/jbi.12611

2015
Rosser, N., Phillimore, A. B., & Mallet, J. (2015). Extensive range overlap between Heliconius sister species: evidence for sympatric speciation in butterflies? BMC Evolutionary Biology , 15, 125.Abstract

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.

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(Open Access) doi:10.1186/s12862-015-0420-3

Keightley, P. D., Pinharanda, A., Ness, R. W., Simpson, F., Dasmahapatra, K. K., Mallet, J., Davey, J. W., et al. (2015). Estimation of the spontaneous mutation rate in Heliconius melpomene. Molecular Biology and Evolution , 32, 239-43.Abstract

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.

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(Open Access) doi:10.1093/molbev/msu302

Kozak, K. M., Wahlberg, N., Neild, A. F., Dasmahapatra, K. K., Mallet, J., & Jiggins, C. D. (2015). Multilocus species trees show the recent adaptive radiation of the mimetic heliconius butterflies. Systematic Biology , 64, 505-24.Abstract

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.

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(Open Access) doi:10.1093/sysbio/syv007

Mallet, J. (2015). New genomes clarify mimicry evolution. Nature Genetics , 47, 306-7.Abstract

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.

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doi: 10.1038/ng.3260.

2014
Mallet, J. (2014). Speciation: frog mimics prefer their own. Current Biology , 24, R1094-R1096.Abstract

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.

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doi:10.1016/j.cub.2014.10.001

Rosser, N., Dasmahapatra, K. K., & Mallet, J. (2014). Stable Heliconius butterfly hybrid zones are correlated with a local rainfall peak at the edge of the Amazon basin. Evolution , 68, 3470-3484.Abstract

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.

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doi:10.1111/evo.12539

2013
Mérot, C., Mavárez, J., Evin, A., Dasmahapatra, K. K., Mallet, J., Lamas, G., & Joron, M. (2013). Genetic differentiation without mimicry shift in a pair of hybridizing Heliconius species (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society , 109, 830-847.Abstract

Butterflies in the genus Heliconius have undergone rapid adaptive radiation for warning patterns and mimicry, andare excellent models to study the mechanisms underlying diversification. In Heliconius, mimicry rings typicallyinvolve distantly related species, whereas closely related species often join different mimicry rings. Genetic andbehavioural studies have shown how reproductive isolation in many pairs of Heliconius taxa is largely mediatedby natural and sexual selection on wing colour patterns. However, recent studies have uncovered new cases inwhich pairs of closely related species are near-perfect mimics of each other. Here, we provide morphometric andgenetic evidence for the coexistence of two closely related, hybridizing co-mimetic species on the eastern slopes ofthe Andes, H. melpomene amaryllis and H. timareta ssp. nov., which is described here as H. timareta thelxinoe.A joint analysis of multilocus genotyping and geometric morphometrics of wing shape shows a high level ofdifferentiation between the two species, with only limited gene flow and mixing. Some degree of genetic mixing canbe detected, but putative hybrids were rare, only one of 175 specimens being a clear hybrid. In contrast, we foundphenotypic differentiation between populations of H. timareta thelxinoe, possibly indicative of strong selection forlocal mimicry in different communities. In this pair of species, the absence of breakdown of genetic isolation despitenear-identical wing patterns implies that factors other than wing patterns keep the two taxa apart, such aschemical or behavioural signals, or ecological adaptation along a strong altitudinal gradient. © 2013 The LinneanSociety of London, Biological Journal of the Linnean Society, 2013

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doi:10.1111/bij.12091

Mallet, J. (2013). Introgression: Brower's criticisms. Part I. New evidence for hybridization and introgression is unsettling. eratosignis. BLOG
Mallet, J. (2013). Introgression: Brower's criticisms. Part II. Itemized critiques by Brower (2012), and comments thereon. eratosignis. BLOG
Merrill, R. M., Naisbit, R. E., Mallet, J., & Jiggins, C. D. (2013). Ecological and genetic factors influencing the transition between host-use strategies in sympatric Heliconius butterflies. Journal of Evolutionary Biology , 26, 1959-67.Abstract

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.

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doi: 10.1111/jeb.12194

Briscoe, A. D., Macias-Munoz, A., Kozak, K. M., Walters, J. R., Yuan, F., Jamie, G. A., Martin, S. H., et al. (2013). Female behaviour drives expression and evolution of gustatory receptors in butterflies. PLoS Genetics , 9 e1003620.Abstract

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.

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(Open Access) doi:10.1371/journal.pgen.1003620

Martin, S. H., Dasmahapatra, K. K., Nadeau, N. J., Salazar, C., Walters, J. R., Simpson, F., Blaxter, M., et al. (2013). Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Research , 23, 1817-1828.Abstract

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.

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(Open Access) doi:10.1101/gr.159426.113

Nadeau, N. J., Martin, S. H., Kozak, K. M., Salazar, C., Dasmahapatra, K. K., Davey, J. W., Baxter, S. W., et al. (2013). Genome-wide patterns of divergence and gene flow across a butterfly radiation. Molecular Ecology , 22, 814-826.Abstract

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.

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doi: 10.1111/j.1365-294X.2012.05730.x

Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J., Bierne, N., Boughman, J., et al. (2013). Hybridization and speciation. Journal of Evolutionary Biology , 26, 229-246.Abstract

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.

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doi:10.1111/j.1420-9101.2012.02599.x

2012
Hill, R. I., Elias, M., Dasmahapatra, K. K., Jiggins, C. D., Koong, V., Willmott, K. R., & Mallet, J. (2012). Ecologically relevant cryptic species in the highly polymorphic Amazonian butterfly Mechanitis mazaeus sensu lato (Lepidoptera: Nymphalidae; Ithomiini). Biological Journal of the Linnean Society , 106, 540-560.Abstract

The understanding of mimicry has relied on a strong biosystematic framework ever since early naturalists firstrecognized this textbook example of natural selection. We follow in this tradition, applying new biosystematicsinformation to resolve problems in an especially difficult genus of tropical butterflies. Mechanitis species areimportant components of Neotropical mimetic communities. However, their colour pattern variability has presentedchallenges for systematists, and has made it difficult to study the very mimicry they so nicely illustrate. The SouthAmerican Mechanitis mazaeus and relatives have remained particularly intractable. Recent systematists haverecognized one highly polytypic species, whereas earlier work recognized the melanic Andean foothill races as adistinct species: Mechanitis messenoides. Recent molecular evidence suggests M. mazaeus and M. messenoides aregenetically well differentiated, but evidence of morphological and ecological differences indicative of separatespecies was still lacking. Thus, it remains to be conclusively demonstrated whether this is an extreme case of apolymorphic mimetic species, or whether distinct co-mimetic lineages are involved. Here we provide evidence thatM. mazaeus and M. messenoides are ecologically distinct and identify consistent morphological differences in bothadult and immature stages. These ecological and morphological differences are correlated with mitochondrialsequence data. In spite of some overlap in almost all traits, wing shape, adult colour pattern, and larval colourpattern differ between the two species, in addition to clutch size and larval host use in local sympatry. Althoughthree well-differentiated mitochondrial DNA (mtDNA) haplogroups were identified within these two species, one forM. mazaeus and two within M. messenoides, no morphological or ecological differences were found between twomtDNA haplogroups, both of which appear to belong to M. messenoides. We conclude that M. mazaeus andM. messenoides are distinct although highly polymorphic species, each with multiple sympatric co-mimetic forms,and suggest that further work is needed to clarify the identity of other phenotypes and subspecies of Mechanitis.© 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 540–560.

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doi:10.1111/j.1095-8312.2012.01874.x

Mallet, J., & Dasmahapatra, K. K. (2012). Hybrid zones and the speciation continuum in Heliconius butterflies. Molecular Ecology , 21, 5643-5645.Abstract

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.

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doi:10.1111/mec.12058

Mallet, J. (2012). The struggle for existence. How the notion of carrying capacity, K, obscures the links between demography, Darwinian evolution and speciation. Evolutionary Ecology Research , 14, 627–665.Abstract

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.

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Rosser, N., Phillimore, A. B., Huertas, B., Willmott, K. R., & Mallet, J. (2012). Testing historical explanations for gradients in species richness in heliconiine butterflies of tropical America. Biological Journal of the Linnean Society , 105, 479-497.Abstract

We compiled a large database of 58 059 point locality records for 70 species and 434 subspecies of heliconiinebutterflies and used these data to test evolutionary hypotheses for their diversification. To study geographicalpatterns of diversity and contact zones, we mapped: (1) species richness; (2) mean molecular phylogenetic terminalbranch length; (3) subspecies richness and the proportion of specimens that were subspecific hybrids, and (4)museum sampling effort. Heliconiine species richness is high throughout the Amazon region and peaks near theequator in the foothills and middle elevations of the eastern Andes. Mean phylogenetic terminal branch length islowest in the eastern Andes and tends to be low in species-rich areas. By contrast, areas of high subspeciesrichness, where subspecies overlap in range and/or hybridize, are concentrated along the course of the AmazonRiver, with the eastern Andes slopes and foothills relatively depauperate in terms of local intraspecific phenotypicdiversity. Spatial gradients in heliconiine species richness in the Neotropics are consistent with the hypothesis thatspecies richness gradients are driven at least in part by variation in speciation and/or extinction rates, resultingin observed gradients in mean phylogenetic branch length, rather than via evolutionary age or niche conservatismalone. The data obtained in the present study, coupled with individual case studies of recently evolved Heliconiusspecies, suggest that the radiation of heliconiine butterflies occurred predominantly on the eastern slopes of theAndes in Colombia, Ecuador, and Peru, as well as in the upper/middle Amazon basin. © 2012 The Linnean Societyof London, Biological Journal of the Linnean Society, 2012, 105, 479–497.

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doi:10.1111/j.1095-8312.2011.01814.x

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