Drift drives phenotypic evolution in a rapid island radiation

Abstract

Understanding the processes that generate phenotypic diversity is central to explaining how new species form1,2. Evolutionary theory predicts that rapid evolution of signaling traits, such as feather coloration, can promote speciation3,4 but empirical support is inconsistent5,6. Phenotypic divergence of such traits is expected during speciation4, but these microevolutionary dynamics are rarely examined at macroevolutionary scales or linked to underlying population demography. Here, we leverage complete taxon sampling across an iconic insular bird radiation that helped shape early theories of allopatric speciation. We integrate whole-genome data with a comprehensive, fine-scale dataset of whole-body plumage coloration to directly test whether signaling trait evolution covaries with lineage diversification and to disentangle the roles of selection and drift. We find that lineages with faster rates of color evolution diversify more rapidly. Strikingly, rates of color evolution accelerate as genomic diversity declines, providing direct evidence that genetic drift--rather than strong sexual or ecological selection--can drive rapid phenotypic change in small, isolated insular populations. Together, these results provide compelling evidence that neutral demographic processes can accelerate the evolution of sexual signals and play a central role in generating phenotypic diversity during island radiations.