Population genomics of the island thrush elucidates one of earth’s great archipelagic radiations
Andrew Hart Reeve, Graham Gower, José Martín Pujolar, Brian Tilston Smith, Bent Petersen, Urban Olsson, Tri Haryoko, Bonny Koane, Gibson Maiah, Mozes P. K. Blom, Per G. P. Ericson, Martin Irestedt, Fernando Racimo, Knud A. Jønsson
Abstract
Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world’s most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush’s success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology. Island radiations are powerful systems for studying evolutionary processes and biodiversity buildup. Here we use population genomics methods to investigate one of the most spectacular and perplexing archipelagic radiations among birds. The island thrush displays a complex mosaic of plumage variation and occupies a vast range across the Indo-Pacific despite being sedentary and largely restricted to mountains. We reconstruct its evolutionary relationships, demographic history, and population structure to provide a detailed picture of an explosive radiation from Asia during the Pleistocene. We illustrate how departure from the mainland and subsequent founder events degraded genetic variation, and detect considerable cross-population gene flow. Our results place focus on the dynamics of populations at the leading edge of radiations vs. those behind it.