Abstract

BackgroundHomo sapiens have experienced admixture many times in the last few thousand years. To examine how admixture affects local adaptation, we investigated genomes of modern Polynesians, who are shaped through admixture between Austronesian-speaking people from Southeast Asia (Asian-related ancestors) and indigenous people in Near Oceania (Papuan-related ancestors).MethodsIn this study local ancestry was estimated across the genome in Polynesians (23 Tongan subjects) to find the candidate regions of admixture-enabled selection contributed by Papuan-related ancestors.ResultsThe mean proportion of Papuan-related ancestry across the Polynesian genome was estimated as 24.6% (SD = 8.63%), and two genomic regions, the extended major histocompatibility complex (xMHC) region on chromosome 6 and the ATP-binding cassette transporter sub-family C member 11 (ABCC11) gene on chromosome 16, showed proportions of Papuan-related ancestry more than 5 SD greater than the mean (> 67.8%). The coalescent simulation under the assumption of selective neutrality suggested that such signals of Papuan-related ancestry enrichment were caused by positive selection after admixture (false discovery rate = 0.045). The ABCC11 harbors a nonsynonymous SNP, rs17822931, which affects apocrine secretory cell function. The approximate Bayesian computation indicated that, in Polynesian ancestors, a strong positive selection (s = 0.0217) acted on the ancestral allele of rs17822931 derived from Papuan-related ancestors.ConclusionsOur results suggest that admixture with Papuan-related ancestors contributed to the rapid local adaptation of Polynesian ancestors. Considering frequent admixture events in human evolution history, the acceleration of local adaptation through admixture should be a common event in humans.

Highlights

  • Homo sapiens have experienced admixture many times in the last few thousand years

  • Our results suggest that the admixture with Papuan-related ancestors contributed to the rapid adaptation of Polynesian ancestors to the environment of Oceania

  • Selection acted on the earwax‐associated SNP on ATP-binding cassette transporter sub-family C member 11 (ABCC11) To evaluate the intensity of positive selection on the ABCC11 gene, we focused on a nonsynonymous SNP (G180R), rs17822931

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Summary

Introduction

Homo sapiens have experienced admixture many times in the last few thousand years. To examine how admixture affects local adaptation, we investigated genomes of modern Polynesians, who are shaped through admixture between Austronesian-speaking people from Southeast Asia (Asian-related ancestors) and indigenous people in Near Oceania (Papuan-related ancestors). The first immigrants settled Sahul, a continent that comprised the land masses of presentday Australia, New Guinea, and the surrounding small islands. They are considered the ancestors of modern Papuans and Aboriginal Australians. They colonized the Isshiki et al BMC Ecol Evo (2021) 21:179 islands of New Britain and New Ireland, reaching the Solomon Islands by 28,000 years ago [65]. This region of initial colonization is known as Near Oceania. Due to the large expanse of ocean to the east of Near Oceania, Remote Oceania, which includes eastern part of the Solomon Islands, Vanuatu, Fiji and all the islands of Polynesia, remained unoccupied until the Late Holocene

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