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Gene flow persists millions of years after speciation in Heliconius butterflies.

ABSTRACT: BACKGROUND: Hybridization, or the interbreeding of two species, is now recognized as an important process in the evolution of many organisms. However, the extent to which hybridization results in the transfer of genetic material across the species boundary (introgression) remains unknown in many systems, as does the length of time after initial divergence that the species boundary remains porous to such gene flow. RESULTS: Here I use genome-wide genotypic and DNA sequence data to show that there is introgression and admixture between the melpomene/cydno and silvaniform clades of the butterfly genus Heliconius, groups that separated from one another as many as 30 million generations ago. Estimates of historical migration based on 523 DNA sequences from 14 genes suggest unidirectional gene flow from the melpomene/cydno clade into the silvaniform clade. Furthermore, genetic clustering based on 520 amplified fragment length polymorphisms (AFLPs) identified multiple individuals of mixed ancestry showing that introgression is on-going. CONCLUSION: These results demonstrate that genomes can remain porous to gene flow very long after initial divergence. This, in turn, greatly expands the evolutionary potential afforded by introgression. Phenotypic and species diversity in a wide variety of organisms, including Heliconius, have likely arisen from introgressive hybridization. Evidence for continuous gene flow over millions of years points to introgression as a potentially important source of genetic variation to fuel the evolution of novel forms.

SUBMITTER: Kronforst MR

PROVIDER: S-EPMC2322973 | biostudies-literature | 2008

REPOSITORIES: biostudies-literature

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Gene flow persists millions of years after speciation in Heliconius butterflies.

Kronforst Marcus R MR

BMC evolutionary biology 20080327

<h4>Background</h4>Hybridization, or the interbreeding of two species, is now recognized as an important process in the evolution of many organisms. However, the extent to which hybridization results in the transfer of genetic material across the species boundary (introgression) remains unknown in many systems, as does the length of time after initial divergence that the species boundary remains porous to such gene flow.<h4>Results</h4>Here I use genome-wide genotypic and DNA sequence data to sh ...[more]

PMID: 18371203

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Project description:BackgroundA key to understanding the origins of species is determining the evolutionary processes that drive the patterns of genomic divergence during speciation. New genomic technologies enable the study of high-resolution genomic patterns of divergence across natural speciation continua, where taxa pairs with different levels of reproductive isolation can be used as proxies for different stages of speciation. Empirical studies of these speciation continua can provide valuable insights into how genomes diverge during speciation.MethodsWe examine variation across a handful of genomic regions in parapatric and allopatric populations of Heliconius butterflies with varying levels of reproductive isolation. Genome sequences were mapped to 2.2-Mb of the H. erato genome, including 1-Mb across the red color pattern locus and multiple regions unlinked to color pattern variation.ResultsPhylogenetic analyses reveal a speciation continuum of pairs of hybridizing races and incipient species in the Heliconius erato clade. Comparisons of hybridizing pairs of divergently colored races and incipient species reveal that genomic divergence increases with ecological and reproductive isolation, not only across the locus responsible for adaptive variation in red wing coloration, but also at genomic regions unlinked to color pattern.DiscussionWe observe high levels of divergence between the incipient species H. erato and H. himera, suggesting that divergence may accumulate early in the speciation process. Comparisons of genomic divergence between the incipient species and allopatric races suggest that limited gene flow cannot account for the observed high levels of divergence between the incipient species.ConclusionsOur results provide a reconstruction of the speciation continuum across the H. erato clade and provide insights into the processes that drive genomic divergence during speciation, establishing the H. erato clade as a powerful framework for the study of speciation.

Project description:The unpalatable and warning-patterned butterflies Heliconius erato and Heliconius melpomene provide the best studied example of mutualistic Müllerian mimicry, thought-but rarely demonstrated-to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of H. erato and H. melpomene, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of H. erato and H. melpomene, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of H. erato and H. melpomene. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of H. erato and H. melpomene show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of H. erato and H. melpomene occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for H. erato relative to H. melpomene and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Müllerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.

Dataset Information

Gene flow persists millions of years after speciation in Heliconius butterflies.

Publications

Gene flow persists millions of years after speciation in Heliconius butterflies.

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