Abstract

How frequent is gene flow between species? The pattern of evolution is typically portrayed as a phylogenetic tree, yet gene flow between good species may be an important mechanism in diversification, spreading adaptive traits and leading to a complex pattern of phylogenetic incongruence. This process has thus far been studied mainly among a few closely related species, or in geographically restricted areas such as islands, but not on the scale of a continental radiation. Using a genomic representation of 40 out of 47 species in the genus, we demonstrate that admixture has played a role throughout the evolution of the charismatic Neotropical butterflies Heliconius. Modeling of phylogenetic networks based on the exome uncovers up to 13 instances of interspecific gene flow. Admixture is detected among the relatives of Heliconius erato, as well as between the ancient lineages leading to modern clades. Interspecific gene flow played a role throughout the evolution of the genus, although the process has been most frequent in the clade of Heliconius melpomene and relatives. We identify Heliconius hecalesia and relatives as putative hybrids, including new evidence for introgression at the loci controlling the mimetic wing patterns. Models accounting for interspecific gene flow yield a more complete picture of the radiation as a network, which will improve our ability to study trait evolution in a realistic comparative framework.

Highlights

  • Interspecific hybridization and the resulting gene flow across porous species barriers are increasingly recognized as major processes in evolution, detectable across the tree of life (Hilario and Gogarten 1993; Feliner et al 2017)

  • We find that admixture between species has been common during the evolution of Heliconius butterflies, and was the mechanism spreading multiple advantageous genes

  • Hybridization might often result in the production of deleterious combinations of alleles at different loci, introgression can enable adaptation by providing novel variation that may be favored by natural selection, as demonstrated in the iconic adaptive radiation of Darwin’s finches (Lamichhaney et al 2015) and in our own lineage (Huerta-Sanchez et al 2014)

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Summary

Introduction

Interspecific hybridization and the resulting gene flow across porous species barriers are increasingly recognized as major processes in evolution, detectable across the tree of life (Hilario and Gogarten 1993; Feliner et al 2017). Hybridization might often result in the production of deleterious combinations of alleles at different loci, introgression can enable adaptation by providing novel variation that may be favored by natural selection, as demonstrated in the iconic adaptive radiation of Darwin’s finches (Lamichhaney et al 2015) and in our own lineage (Huerta-Sanchez et al 2014).

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