Patterns of genetic divergence and demographic history shed light on island‐mainland population dynamics and melanic plumage evolution in the white‐winged Fairywren*

Abstract

The existence of distinct traits in island versus mainland populations offers opportunities to gain insights into how eco‐evolutionary processes operate under natural conditions. We used two island colonization events in the white‐winged fairywren (Malurus leucopterus) to investigate the genomic and demographic origin of melanic plumage. This avian species is distributed across most of Australia, and males of the mainland subspecies (M. l. leuconotus) exhibit a blue nuptial plumage in contrast to males of two island subspecies – M. l. leucopterus on Dirk Hartog Island and M. l. edouardi on Barrow Island – that exhibit a black nuptial plumage. We used reduced‐representation sequencing to explore differentiation and demographic history in this species and found clear patterns of divergence between mainland and island populations, with additional substructuring on the mainland. Divergence between the mainland and Dirk Hartog was approximately 10 times more recent than the split between the mainland and Barrow Island, supporting two independent colonizations. In both cases, estimated gene flow between the mainland and the islands was low, contributing to signals of divergence among subspecies. Our results present demographic reconstructions of mainland‐island dynamics and associated plumage variation in white‐winged fairywrens, with broader implications regarding our understanding of convergent evolution in insular populations.

The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

“…Our phylogenomic and population genomic analysis indicate that the divergence of White-shouldered Fairywren populations throughout New Guinea occurred within approximately the last 800,000 years. Reduced genetic diversity in black and pied populations, relative to the brown population, indicates that each population may have experienced a bottleneck following this expansion, which highlights the poor dispersal capabilities of fairywrens (Rowley and Russell 1997;Walsh et al 2021) and the strength of lowland biogeographic barriers in New Guinea (Marki et al 2018). All immediate relatives among Malurus fairywrens, including the sister species M. melanocephalus, are characterized by cryptic brown plumage in females, and our phylogenetic reconstruction is consistent with the ancestral females of extant White-shouldered Fairywren populations lacking ornamentation and a single evolutionary origin of black and pied female ornamentation (Fig.…”

“…Reduced genetic diversity in black and pied populations, relative to the brown population, indicates that each population may have experienced a bottleneck following this expansion, which highlights the poor dispersal capabilities of fairywrens (Rowley and Russell 1997; Walsh et al. 2021) and the strength of lowland biogeographic barriers in New Guinea (Marki et al. 2018).…”

Digest: Population genomics reveals convergence toward melanism in different island populations

“…In this issue, Walsh et al. (2021) take advantage of the mainland and island populations of white‐winged fairywrens ( Malurus leucopterus ) to study the evolution of plumage traits. This species can be found across most of Australia and has been classified into several subspecies.…”

“…Using genomic and demographic analyses, Walsh et al. (2021) revealed that the divergence between the mainland population and the Dirk Hartog Island population was more recent (ca. 173,000 generations ago) than the divergence between the mainland population and Barrow Island population (about 1.75 million generations ago).…”

“…Walsh et al. (2021) proposed that the “more likely evolutionary driver of melanic plumage in insular populations of white‐winged fairywrens may be natural or indirect selection” through pleiotropy. Indeed, sexual selection is expected to be weaker on islands because lower genetic diversity should reduce the indirect benefits of mate choice.…”