Selective sweeps on different pigmentation genes mediate convergent evolution of island melanism in two incipient bird species

Insular organisms often evolve predictable phenotypes, like flightlessness, extreme body sizes, or increased melanin deposition. The evolutionary forces and molecular targets mediating these patterns remain mostly unknown. Here we study the Chestnut-bellied Monarch (Monarcha castaneiventris) from the Solomon Islands, a complex of closely related subspecies in the early stages of speciation. On the large island of Makira M. c. megarhynchus has a chestnut belly, whereas on the small satellite islands of Ugi, and Santa Ana and Santa Catalina (SA/SC) M. c. ugiensis is entirely iridescent blue-black (i.e., melanic). Melanism has likely evolved twice, as the Ugi and SA/SC populations were established independently. To investigate the genetic basis of melanism on each island we generated whole genome sequence data from all three populations. Non-synonymous mutations at the MC1R pigmentation gene are associated with melanism on SA/SC, while ASIP, an antagonistic ligand of MC1R, is associated with melanism on Ugi. Both genes show evidence of selective sweeps in traditional summary statistics and statistics derived from the ancestral recombination graph (ARG). Using the ARG in combination with machine learning, we inferred selection strength, timing of onset and allele frequency trajectories. MC1R shows evidence of a recent, strong, soft selective sweep. The region including ASIP shows more complex signatures; however, we find evidence for sweeps in mutations near ASIP, which are comparatively older than those on MC1R and have been under relatively strong selection. Overall, our study shows convergent melanism results from selective sweeps at independent molecular targets, evolving in taxa where coloration likely mediates reproductive isolation with the neighboring chestnut-bellied subspecies. Author summary Chestnut-bellied Monarchs (Monarcha castaneiventris ugiensis) from two archipelagos in the Solomon Islands have evolved entirely black plumage from a chestnut ancestor (Monarcha castaneiventris megarhynchus), a phenomenon known as island melanism. We obtain and analyze whole genome sequences using traditional summary statistics and new methods that combine inference of the ancestral recombination graph with machine learning. We find multiple lines of evidence for independent selective sweeps on the MC1R and ASIP genes, a receptor/ligand pair which regulates the production of melanin. Melanism on each archipelago is mediated by mutations in one of these two genes. Mutations in and around MC1R underwent a recent soft sweep experiencing strong selection on the islands of Santa Ana and Santa Catalina, whereas selection was also strong but comparatively older for ASIP on the island of Ugi. We show how melanism originated under positive selection on independent molecular targets, evolving convergently in taxa where coloration mediates reproductive isolation.