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Summary Multiple lines of evidence show that modern humans interbred with archaic Denisovans. Here, we report an account of shared demographic history between Australasians and Denisovans distinctively in Island Southeast Asia. Our analyses are based on ∼2.3 million genotypes from 118 ethnic groups of the Philippines, including 25 diverse self-identified Negrito populations, along with high-coverage genomes of Australopapuans and Ayta Magbukon Negritos. We show that Ayta Magbukon possess the highest level of Denisovan ancestry in the world—∼30%–40% greater than that of Australians and Papuans—consistent with an independent admixture event into Negritos from Denisovans. Together with the recently described Homo luzonensis, we suggest that there were multiple archaic species that inhabited the Philippines prior to the arrival of modern humans and that these archaic groups may have been genetically related. Altogether, our findings unveil a complex intertwined history of modern and archaic humans in the Asia-Pacific region, where distinct Islander Denisovan populations differentially admixed with incoming Australasians across multiple locations and at various points in time., Highlights • Comprehensive analyses of archaic ancestry among 118 Philippine ethnic groups • Ayta Magbukon display ∼30%–40% greater Denisovan ancestry than Australopapuans • The model is explained by a distinct admixture event into Negritos from Denisovans • Prior to modern humans, Islander Denisovans may have been present in the Philippines, Larena et al. reveal Philippine Ayta to possess the highest level of Denisovan ancestry in the world—∼30%–40% greater than that of Australopapuans—consistent with an independent admixture event into Negritos from Denisovans. The Philippine archipelago is thus likely inhabited by multiple archaic groups prior to the arrival of modern humans.

Significance A key link to understand human history in Island Southeast Asia is the Philippine archipelago and its poorly investigated genetic diversity. We analyzed the most comprehensive set of population-genomic data for the Philippines: 1,028 individuals covering 115 indigenous communities. We demonstrate that the Philippines were populated by at least five waves of human migration. The Cordillerans migrated into the Philippines prior to the arrival of rice agriculture, where some remain as the least admixed East Asians carrying an ancestry shared by all Austronesian-speaking populations, thereby challenging an exclusive out-of-Taiwan model of joint farming–language–people dispersal. Altogether, our findings portray the Philippines as a crucial gateway, with a multilayered history, that ultimately changed the genetic landscape of the Asia-Pacific region., Island Southeast Asia has recently produced several surprises regarding human history, but the region’s complex demography remains poorly understood. Here, we report ∼2.3 million genotypes from 1,028 individuals representing 115 indigenous Philippine populations and genome-sequence data from two ∼8,000-y-old individuals from Liangdao in the Taiwan Strait. We show that the Philippine islands were populated by at least five waves of human migration: initially by Northern and Southern Negritos (distantly related to Australian and Papuan groups), followed by Manobo, Sama, Papuan, and Cordilleran-related populations. The ancestors of Cordillerans diverged from indigenous peoples of Taiwan at least ∼8,000 y ago, prior to the arrival of paddy field rice agriculture in the Philippines ∼2,500 y ago, where some of their descendants remain to be the least admixed East Asian groups carrying an ancestry shared by all Austronesian-speaking populations. These observations contradict an exclusive “out-of-Taiwan” model of farming–language–people dispersal within the last four millennia for the Philippines and Island Southeast Asia. Sama-related ethnic groups of southwestern Philippines additionally experienced some minimal South Asian gene flow starting ∼1,000 y ago. Lastly, only a few lowlanders, accounting for