Papers

2013
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

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

Heliconius_Genome_Consortium,. (2012). Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature , 487, 94-98.Abstract

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.

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doi: 10.1038/nature11041

Boenigk, J., Ereshefsky, M., Hoef-Emden, K., Mallet, J., & Bass, D. (2012). Concepts in protistology: species definitions and boundaries. European Journal of Protistology , 48, 96-102.Abstract

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.

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doi: 10.1016/j.ejop.2011.11.004

Merrill, R. M., Wallbank, R. W., Bull, V., Salazar, P. C., Mallet, J., Stevens, M., & Jiggins, C. D. (2012). Disruptive ecological selection on a mating cue. Proceedings of the Royal Society B: Biological Sciences , 279, 4907-4913.Abstract

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.

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doi: 10.1098/rspb.2012.1968

Nadeau, N. J., Martin, S. H., Kozak, K. M., Salazar, C., Dasmahapatra, K. K., Davey, J. W., Baxter, S. W., et al. (2012). 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

Nadeau, N. J., Whibley, A., Jones, R. T., Davey, J. W., Dasmahapatra, K. K., Baxter, S. W., Quail, M. A., et al. (2012). Genomic islands of divergence in hybridizing Heliconius butterflies identified by large-scale targeted sequencing. Philosophical Transactions of the Royal Society B , 367, 343-53.Abstract

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.

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doi: 10.1098/rstb.2011.0198

Cook, L. M., Grant, B. S., Saccheri, I. J., & Mallet, J. (2012). Selective bird predation on the peppered moth: the last experiment of Michael Majerus. Biology Letters , 8 609-612.Abstract

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.

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(Open Access) doi: 10.1098/rsbl.2011.1136

Kronforst, M. R., Barsh, G. S., Kopp, A., Mallet, J., Monteiro, A., Mullen, S. P., Protas, M., et al. (2012). Unraveling the thread of nature's tapestry: the genetics of diversity and convergence in animal pigmentation. Pigment Cell and Melanoma Research , 25, 411-433.Abstract

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.

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(Open Access) doi: 10.1111/j.1755-148X.2012.01014.x

2011
Mallet, J. & Dasmahapatra, K. (2011). Catfish mimics (News and Views on Alexandrou et al. article in same issue). Nature , 469, 41-42.Abstract

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.

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Mallet, J., Wynne, I. R., & Thomas, C. D. (2011). Hybridisation and climate change: brown argus butterflies in Britain (Polyommatus subgenus Aricia). Insect Conservation and Diversity , 4 192-199. REPRINT
De-Silva, D. L., VÁSquez, A. S., & Mallet, J. (2011). Selection for enemy-free space: eggs placed away from the host plant increase survival of a neotropical ithomiine butterfly. Ecological Entomology , 36, 667-672.Abstract

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.

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Hines, H. M., Counterman, B. A., Papa, R., Albuquerque de Moura P,, Cardoso, M. Z., Linares, M., Mallet J,, et al. (2011). A wing patterning gene redefines the mimetic history of Heliconius butterflies. Proceedings of the National Academy of Sciences, USA , 108, 19666-19671.Abstract

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.

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2010
Dasmahapatra, K. K., Lamas, G., Simpson, F., & Mallet, J. (2010). The anatomy of a 'suture zone' in Amazonian butterflies: a coalescent-based test for vicariant geographic divergence and speciation. Molecular Ecology , 19, 4283-4301.Abstract

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.

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(Open Access) doi: 10.1111/j.1365-294X.2010.04802.x

Gourbiere, S., & Mallet, J. (2010). Are species real? The shape of the species boundary with exponential failure, reinforcement, and the "missing snowball". Evolution , 64, 1-24.Abstract

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.

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doi: 10.1111/j.1558-5646.2009.00844.x

Counterman, B. A., Araujo-Perez, F., Hines, H. M., Baxter, S. W., Morrison, C. M., Lindstrom, D. P., Papa, R., et al. (2010). Genomic hotspots for adaptation: the population genetics of Mullerian mimicry in Heliconius erato. PLoS Genetics , 6(2), e1000796.Abstract

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.

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doi: 10.1371/journal.pgen.1000796

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