Abstract

BackgroundAlthough hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation. The butterfly genus Heliconius is an excellent system to study hybridization and introgression but most studies have focused on closely related species such as H. cydno and H. melpomene. Here we characterize genome-wide patterns of introgression between H. besckei, the only species with a red and yellow banded ‘postman’ wing pattern in the tiger-striped silvaniform clade, and co-mimetic H. melpomene nanna.ResultsWe find a pronounced signature of putative introgression from H. melpomene into H. besckei in the genomic region upstream of the gene optix, known to control red wing patterning, suggesting adaptive introgression of wing pattern mimicry between these two distantly related species. At least 39 additional genomic regions show signals of introgression as strong or stronger than this mimicry locus. Gene flow has been on-going, with evidence of gene exchange at multiple time points, and bidirectional, moving from the melpomene to the silvaniform clade and vice versa. The history of gene exchange has also been complex, with contributions from multiple silvaniform species in addition to H. besckei. We also detect a signature of ancient introgression of the entire Z chromosome between the silvaniform and melpomene/cydno clades.ConclusionsOur study provides a genome-wide portrait of introgression between distantly related butterfly species. We further propose a comprehensive and efficient workflow for gene flow identification in genomic data sets.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-016-0889-0) contains supplementary material, which is available to authorized users.

Highlights

  • Hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation

  • Recent examples suggest modern humans have benefited by adaptive introgression from different populations and extinct species: introgressed Neanderthal alleles may have helped modern humans adapt to non-African environments [12, 13], and high-altitude adaptive traits have been contributed to Tibetans from Denisovans and Nepalese Sherpa [14, 15]

  • Whole genome phylogenetic analyses We first characterized the evolutionary history of Heliconius butterflies using genome-wide single nucleotide polymorphism (SNP) data from 73 butterflies representing 29 species (Fig. 2)

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Summary

Introduction

Hybridization is thought to be relatively rare in animals, the raw genetic material introduced via introgression may play an important role in fueling adaptation and adaptive radiation. Hybridization can lead to adaptive introgression by transmitting beneficial alleles between species via backcross hybrids [2,3,4], which can happen during either sympatric speciation or the secondary contact phase of allopatric speciation. There are a number of striking examples of adaptive introgression in plants, both between hybridizing wild species as well as between crops and their wild relatives [5,6,7]. Recent examples suggest modern humans have benefited by adaptive introgression from different populations and extinct species: introgressed Neanderthal alleles may have helped modern humans adapt to non-African environments [12, 13], and high-altitude adaptive traits have been contributed to Tibetans from Denisovans and Nepalese Sherpa [14, 15]

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