A Phylogenomic Assessment of Processes Underpinning Convergent Evolution in Open-Habitat Chats

Abstract

Insights into the processes underpinning the evolution of phenotypic parallelism contribute to our understanding of the contributions of ancestral, introgressed, and novel genetic variation to phenotypic evolution. Phylogenomic analyses characterizing genome-wide gene tree heterogeneity can provide first clues about the extent of ILS and of introgression and thereby into the potential of these processes or (in their absence) the need to invoke novel mutations to underpin phenotypic parallelism. Here, we were interested in understanding the trajectories along which phenotypic parallelism may have evolved in open-habitat chats (wheatears of the genus Oenanthe and their relatives). To this end, based on whole-genome resequencing data from 50 taxa of 44 species, we established the species tree, characterized gene tree heterogeneity, and investigated the footprints of ILS and introgression within the latter. The species tree corroborates the evidence for abundant phenotypic parallelism, especially in wheatears. The high levels of gene tree heterogeneity in wheatears are explained by ILS alone only for 30% of internal branches. For multiple branches with high gene tree heterogeneity, D-statistics and phylogenetic networks identified footprints of introgression. Finally, long branches without extensive ILS between clades sporting similar phenotypes provide suggestive evidence for a role of novel mutations in the evolution of these phenotypes. Together, our results suggest that phenotypic parallelism in open-habitat chats evolved along diverse trajectories and highlight that phenotypic diversification is often complex and best depicted as a network of interacting lineages.