Standing genetic variation and de novo mutations underlie parallel evolution of island bird phenotypes

Abstract

Parallel evolution occurs when the same trait evolves in closely related lineages in response to similar ecological contexts and provides some of the best examples of determinism in evolutionary biology. However, from a genetic standpoint, this process can be driven by either new mutations that appear independently in each diverging population or by selection on existing genetic variation common to both lineages. Small-bodied birds, for example, tend to increase in size after they colonise a new island, following what is known as the island rule. Such is the case of the silvereye (Zosterops lateralis), a prolific natural coloniser of southwest Pacific islands. Island forms of this bird species increase in body size after they establish, with the pattern and pace of change consistent with directional natural selection and evident even in the most recent colonisations within the last 200 years. The system provides an exceptional opportunity to explore the genomic basis of repeated body size evolution. We sequenced 377 whole genomes from 31 different silvereye populations, which revealed that both mechanisms are at play: in some lineages, new mutations are highly associated with body and bill size, but there are also highly associated polymorphisms present across all populations. Our research sheds light on the genomic basis of repeated body size evolution and emphasises that multiple molecular mechanisms can underlie similar evolutionary trajectories even within a single taxon.