Major patterns in the introgression history of Heliconius butterflies

Abstract

Gene flow between species, although usually deleterious, is an important evolutionary process that can facilitate adaptation and lead to species diversification. It also makes estimation of species relationships difficult. Here, we use the full-likelihood multispecies coalescent (MSC) approach to estimate species phylogeny and major introgression events in Heliconius butterflies from whole-genome sequence data. We obtain a robust estimate of species branching order among major clades in the genus, including the ‘melpomene-silvaniform’ group, which shows extensive historical and ongoing gene flow. We obtain chromosome-level estimates of key parameters in the species phylogeny, including species divergence times, present-day and ancestral population sizes, as well as the direction, timing, and intensity of gene flow. Our analysis leads to a phylogeny with introgression events that differ from those obtained in previous studies. We find that Heliconius aoede most likely represents the earliest-branching lineage of the genus and that ‘silvaniform’ species are paraphyletic within the melpomene-silvaniform group. Our phylogeny provides new, parsimonious histories for the origins of key traits in Heliconius, including pollen feeding and an inversion involved in wing pattern mimicry. Our results demonstrate the power and feasibility of the full-likelihood MSC approach for estimating species phylogeny and key population parameters despite extensive gene flow. The methods used here should be useful for analysis of other difficult species groups with high rates of introgression.