Full-likelihood genomic analysis clarifies a complex history of species divergence and introgression: the example of the erato-sara group of Heliconius butterflies

Introgression plays a key role in adaptive evolution and species diversification in many groups of species including Heliconius butterflies. However, frequent hybridization and gene flow between species makes estimation of the species phylogeny challenging, especially for rapidly speciating species within adaptive radiations. Here, we analyze the genomic sequences from six members of the erato-sara clade of Heliconius butterflies to infer the species phylogeny and cross-species introgression events. To avoid heterozygote phasing errors in haploid sequences commonly produced by genome assembly methods, we processed and compiled unphased diploid sequence alignments, with the analytical methods averaging over uncertainties in heterozygote phase resolution. We use likelihood-based methods under the multispecies coalescent (MSC) model with and without gene flow to accommodate random fluctuations in genealogical history across the genome due to deep coalescence. There is robust evidence of introgression across the genome, both among distantly related species deep in the phylogeny and between sister species in shallow parts of the tree. We obtain estimates of population parameters such as introgression times and probabilities, species divergence times, and population sizes for modern and ancestral species. We confirm ancestral gene flow between the sara clade and an ancestral population of likely hybrid origin of H. telesiphe, a likely hybrid origin of H. hecalesia, and gene flow between the sister species H. erato and H. himera. Our approach also demonstrates how introgression among ancestral species can explain the history of two chromosomal inversions deep in the phylogeny of the group. For the first time, we not only test for the presence of cross-species gene flow, but also estimate its direction, timing and magnitude, extracting rich historical information of species divergence and gene flow from genomic data