Genome sequences are known for two archaic hominins—Neanderthals and Denisovans—which interbred with anatomically modern humans as they dispersed out of Africa. We identified high-confidence archaic haplotypes in 161 new genomes spanning 14 island groups in Island Southeast Asia and New Guinea and found large stretches of DNA that are inconsistent with a single introgressing Denisovan origin. Instead, modern Papuans carry hundreds of gene variants from two deeply divergent Denisovan lineages that separated over 350 thousand years ago. Spatial and temporal structure among these lineages suggest that introgression from one of these Denisovan groups predominantly took place east of the Wallace line and continued until near the end of the Pleistocene. A third Denisovan lineage occurs in modern East Asians. This regional mosaic suggests considerable complexity in archaic contact, with modern humans interbreeding with multiple Denisovan groups that were geographically isolated from each other over deep evolutionary time.
Contact between modern humans and archaic hominins in the distant past has left a distinctive genetic signature in all human populations alive today. Modern humans interbred with multiple hominin species in different places around the world, including Neanderthals (Green et al., 2010
), Denisovans (Reich et al., 2010
), and possibly others (Hammer et al., 2011
,Mondal et al., 2016
). Examining genome sequences to identify regions that introgressed from these archaic species has revealed evolutionarily adaptive variants and extended deserts of introgression (Sankararaman et al., 2016
,Vernot et al., 2016
). Recently, analysis of Denisovan ancestry in populations across Eurasia uncovered introgression from an extra branch on the Denisovan hominin clade in East Asia (
Browning et al., 2018
). However, the center of gravity of Denisovan admixture today lies >8,000 km south of Denisova Cave in the Papuan populations of tropical eastern Indonesia and New Guinea, where the composition of Denisovan introgression remains poorly understood.
We therefore analyzed archaic introgression in a new dataset covering Island Southeast Asia (ISEA) and Papua, a maritime zone of densely inhabited archipelagos larger than Europe. This culturally and linguistically diverse region remains strikingly underrepresented in modern genetic surveys, despite its extraordinary human diversity and is a major missing link for medical and evolutionary studies (Horton, 2016
). Notably, the area has some of the first traces of anatomically modern humans in Eurasia (Barker et al., 2007
), archaic H. floresiensis
likely coexisted with modern humans here (Sutikna et al., 2016
), and eastern Indonesians, Papuans, and Philippine “negritos,” together with Siberians and South and East Asians, are among the few living groups with substantial traces of archaic introgression from Denisovans (Jinam et al., 2017
,Reich et al., 2011
,Tucci et al., 2018
First, our data suggest that the D1 Denisovans, in contrast to D2, contributed additional DNA to the mainland New Guinea population after the mainland and Baining populations diverged from their common Papuan ancestor (Figure 5
E). This, together with the nearly complete absence of D1 in continental Asia, is most consistent with the scenario that D1 Denisovans were present in New Guinea or East ISEA (e.g., Wallacea). In turn, this would imply that at least some Denisovan populations had the ability to cross large bodies of water, such as the one represented by the Wallace Line. This idea does not seem implausible given archaeological evidence of archaic hominin dispersals—notably, the discovery of stone tools in the Philippines dating to 700 kya (Ingicco et al., 2018
) and the related finding of H. floresiensis
on the island of Flores (Brown et al., 2004
), both across substantial water boundaries that persisted throughout the Pleistocene. Such geographical barriers would limit gene flow and might help to explain the extent of divergence between the D1 Denisovan population and other Denisovan groups.
Second, the late date for the D1 introgression and geographic structure in modern populations suggests that Denisovans survived until 30 kya, and perhaps as recently as 14.5 kya. This is longer than Neanderthals, who died out around 40 kya (
Higham et al., 2014
), or H. floresiensis
, which recent dating suggests did not persist on Flores beyond 50–60 kya (Sutikna et al., 2016
). The implication is that Denisovans living in ISEA may have been among the last of all the archaic hominins to survive. This provides an argument to screen for Denisovan remains possibly misclassified as other hominins in existing archaeological collections and encourages more archaeological research in the poorly accessible and hence incredibly understudied New Guinea region.
Third, the combined evidence of geographic structure and a recent D1 introgression date suggest that Denisovan introgression did not occur immediately following the first modern human settlement in the region (45–50 kya) (O’Connell et al., 2018). This implies that introgression with archaic hominins may not be an inevitable and immediate result of joint occupation of the same territory.
The genetic diversity within the Denisovan clade is consistent with their deep divergence and separation into at least three geographically disparate branches, with one contributing an introgression signal in Oceania and to a lesser extent across Asia (D2), another apparently restricted to New Guinea and nearby islands (D1), and a third in East Asia and Siberia (D0). This suggests that Denisovans were capable of crossing major geographical barriers, including the persistent sea lanes that separated Asia from Wallacea and New Guinea. They therefore spanned an incredible diversity of environments, from temperate continental steppes to tropical equatorial islands. The emerging picture suggests that far from moving into sparsely inhabited country, modern humans experienced repeated and persistent interactions as they expanded out of Africa into this highly structured archaic landscape across Eurasia. This genetic contact yielded a rich legacy, including hundreds of gene variants that continue to contribute to the adaptive success of anatomically modern humans today.