Admixture with indigenous people helps local adaptation: admixture-enabled selection in Polynesians

Mariko Isshiki; Izumi Naka; Ryosuke Kimura; Nao Nishida; Takuro Furusawa; Kazumi Natsuhara; Taro Yamauchi; Minato Nakazawa; Takafumi Ishida; Tsukasa Inaoka; Yasuhiro Matsumura; Ryutaro Ohtsuka; Jun Ohashi

doi:10.1186/s12862-021-01900-y

Admixture with indigenous people helps local adaptation: admixture-enabled selection in Polynesians

BMC Ecol Evol. 2021 Sep 22;21(1):179. doi: 10.1186/s12862-021-01900-y.

Authors

Affiliations

¹ Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, 113-0033, Japan.
² Department of Human Biology and Anatomy, Graduate School of Medicine, University of the Ryukyus, Nishihara, 903-0125, Japan.
³ Genome Medical Science Project, Research Center for Hepatitis and Immunology, National Center for Global Health and Medicine, Chiba, 272-8516, Japan.
⁴ Graduate School of Asian and African Area Studies, Kyoto University, Kyoto, 606-8501, Japan.
⁵ Department of International Health and Nursing, Faculty of Nursing, Toho University, Tokyo, 143-0015, Japan.
⁶ Faculty of Health Sciences, Hokkaido University, Sapporo, 060-0812, Japan.
⁷ Graduate School of Health Sciences, Kobe University, Kobe, 654-0142, Japan.
⁸ Department of Human Ecology, Faculty of Agriculture, Saga University, Saga, 840-8502, Japan.
⁹ Faculty of Health and Nutrition, Bunkyo University, Chigasaki, 253-8550, Japan.
¹⁰ Japan Wildlife Research Center, Tokyo, 130-8606, Japan.
¹¹ Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo, 113-0033, Japan. juno-tky@umin.ac.jp.

Abstract

Background: 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).

Methods: In 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.

Results: The 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.

Conclusions: Our 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.

Keywords: Admixture; Admixture-enabled selection; Genetic ancestry; Polynesia; Population genomics; Positive selection; Rapid adaptation.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

ATP-Binding Cassette Transporters
Adaptation, Physiological*
Bayes Theorem
Humans
Indigenous Peoples
Native Hawaiian or Other Pacific Islander* / genetics
Oceania

Substances

ABCC11 protein, human
ATP-Binding Cassette Transporters