Gene flow persists millions of years after speciation in Heliconius butterflies

Marcus R Kronforst

doi:10.1186/1471-2148-8-98

Abstract

BackgroundHybridization, 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.ResultsHere 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.ConclusionThese 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.

Highlights

Hybridization, or the interbreeding of two species, is recognized as an important process in the evolution of many organisms
Historical migration inferred from DNA sequence data In order to examine rates of gene flow between the two clades, I sequenced multiple haplotypes for one mitochondrial and 13 nuclear genes from three species in the melpomene/cydno clade (H. cydno, H. pachinus, H. melpomene) and one species in the silvaniform clade (H. hecale)
For the comparisons involving H. pachinus and H. melpomene, the 90% highest posterior density interval for this function did not include zero, allowing rejection of the no gene flow hypothesis. These results, which are suggestive of unidirectional gene flow from the melpomene/cydno clade into the silvaniform clade, are consistent with the observation that of the two suspected backcross hybrids that have been collected in the field, both are believed to have resulted from backcrossing in the direction of the silvaniform clade parent (H. melpomene × H. ethilla backcrossed to H. ethilla) [25,27]

Summary

Introduction

Hybridization, or the interbreeding of two species, is recognized as an important process in the evolution of many organisms. Surveys of hybridization in animals show that it occurs predominantly between closely-related sister species [5], and well-characterized examples of interspecific gene flow generally involve species that diverged very recently [10,11,12,13]. These observations are consistent with theory and data which show that genetic incompatibilities that result in hybrid sterility and inviability accumulate as species diverge [14]. In turn, reduce or eliminate the opportunity for gene exchange Despite these general trends, there are occasional examples of hybridi-

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