Chronology of Natural Selection in Human Genomes From Wallacea and North Sahul

Nicolas Brucato1, André Mathilde2, Georgi Hudjashov2, Mayukh Mondal2, Murray Cox3, Matthew Leavesley4,5,6, Francois-Xavier Ricaut1

1Laboratoire Evolution et Diversite Biologique (EDB UMR 5174), Universite de Toulouse Midi-Pyrénées, CNRS, IRD, France

2Institute of Genomics, University of Tartu, Estonia

3School of Natural Sciences, Massey University, New Zealand

4Strand of Anthropology, Sociology and Archaeology, School of Humanities & Social Sciences, University of Papua New Guinea, Papua New Guinea

5College of Arts, Society and Education, James Cook University, Australia

6ARC Centre of Excellence for Australian Biodiversity and Heritage, University of Wollongong, Australia

As human populations left Asia to first settle Oceania around 50,000 years ago, they entered a territory ecologically separated from the Old World for millions of years. New Guinea and Australia were then joined into an ancient continent, Sahul, comprising a unique ecosystem that certainly represented an evolutionary challenge for the first settlers. We analyzed genomic data of 239 modern Oceanian individuals to detect and date signals of selection specific to this region. Combining both relative and absolute dating approaches, we identified a strong pattern of genetic adaptations between 52,000 and 54,000 years ago in the genomes of descendants of the first settlers of Sahul. This strikingly corresponds to the dates of initial settlement as inferred from archaeological evidence. Genetic fragments under selection during this period, some showing enrichment in Denisovan ancestry, overlap genes involved in the immune response and diet, especially based on plants. Pathogens and natural resources, especially from endemic plants, therefore appear to have acted as strong selective pressures on the genomes of the first settlers of Sahul.