COMMENTARY NeanderthalsandDenisovansasbiologicalinvaders COMMENTARY John Hawksa,1 Humans stand out among our close primate relatives A growing synthesis of fossil and genetic data as effective biological invaders. Our recent history has reveals the striking dynamism of these archaic people. included range expansions into remote and harsh Regional-scale dispersals among Neanderthals of geographic regions, and invasions by some popula- the past 100,000 y may explain mitochondrial DNA tions into areas long occupied by others. Historians (mtDNA) clade turnover at sites across Europe (6). In- tend to frame these events as a story of technolog- dividual genomes show inbreeding and decline in ical and economic progress, while admitting that local populations, but the variation across the Ne- disease sometimes plays a central part—atriad anderthal range was relatively greater than across made memorable by Guns, Germs, and Steel: The human populations occupying similar regions today Fates of Human Societies (1). Ancient DNA is reveal- (7). An early Neanderthal population represented at ing a deeper prehistory of human dispersals, however, Sima de los Huesos, Spain, had different mtDNA showing continuity with invasions as understood by from any later Neanderthals (8), meaning that all later biologists, not just historians. Now, in PNAS, Rogers Neanderthals inherited their mtDNA from a second et al. (2) find that not only modern humans but also episode of invasion and introgression from Africa (9). Neanderthals and Denisovans may share a surprisingly A later episode of introgression into Neanderthals invasive origin. from early modern humans is evidenced in Central The story of Neanderthal and Denisovan origins Asia, but not later European Neanderthals (10). This has developed rapidly during the past 7 y. Two high- already-complex picture depicts only the northern coverage genomes, and more fragmentary genome tier of the Neanderthal range and likely undersam- data from a handful of other individuals, have yielded ples their variation; the morphologically diverse Late powerful insights about the diversity of these ancient Pleistocene Neanderthals of Southwest Asia have not groups and their legacy of genetic introgression into yet yielded ancient DNA evidence. recent humans (3). These archaic populations share a The Denisovans likewise had low local variation deep common history, and individual genomes record and high regional differentiation, evidenced by the a history of high inbreeding and low gene flow across genetic distance between the high-coverage genome their ancient geographic ranges (4, 5). In their new of Denisova 3 and the Denisovan lineages that study, Rogers et al. (2) find that the common ancestral introgressed into the ancestors of Melanesian and population of the Denisovans and Neanderthals under- Australian peoples (5). Ancient DNA evidence of Deni- went a tight bottleneck, immediately after this popu- sovans comes only from Denisova Cave itself, but lation diverged from the African ancestors of modern population turnover is suggested by the high mtDNA humans. This bottleneck was rapid, maybe only 300 and nuclear genome divergence of earlier and later generations, and the Neanderthal and Denisovan specimens from this single site (11). The latest Deni- populations separated quickly thereafter. sovans received introgression both from Neanderthals This archaic human dispersal, which unfolded more and from an as-yet-unknown genetically divergent than 600 ka, bears a striking parallel to the much later ghost population (4). dispersal of modern humans from Africa into Eurasia What made Neanderthals and Denisovans suc- after 100 ka. In both cases, the small bottleneck is cessful invaders? Twenty years ago, some archae- etched into the genomes of all their descendants, and ologists thought that the origin of both Neanderthal in both cases, this founder population quickly ex- and modern human populations could be aligned panded its geographic range and divided into regional with the origin and dispersal of technology. In this populations. Far from the stereotype of plodding, view, Neanderthals and modern humans emerged retrograde cavemen, the Neanderthals exhibited around 300 ka, at around the same time that explosive dispersal and growth. Levallois reduction strategies supplanted the earlier aDepartment of Anthropology, University of Wisconsin–Madison, Madison, WI 53706-1193 Author contributions: J.H. wrote the paper. The author declares no conflict of interest. See companion article on page 9859. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1713163114 PNAS | September 12, 2017 | vol. 114 | no. 37 | 9761–9763 Downloaded by guest on September 27, 2021 Acheulean. In this hypothesis, the Neanderthals built upon a a metapopulation of ancient humans, cooperativeness may have Levallois technical heritage by developing Mousterian indus- fluctuated across groups with different levels of connectivity tries in western Eurasia, and ancestral modern humans de- and shared ancestry, declining as biological distance and veloped Middle Stone Age (MSA) industries in Africa. Modern intergroup aggression increased. Initially small, growing humans within Africa gradually developed yet more advanced groups with high initial consanguinity might easily invade technology based upon blades, which ultimately enabled such a metapopulation. a small group of them to invade Eurasia, supplanting the Neanderthals. Pathogen Relaxation This hypothesis, still found in some textbooks, no longer fits Prehistoric evidence about pathogens is sparse, and it was long the data. Genetic dates carry much uncertainty, but Neanderthals, assumed that epidemic diseases with high mortality costs only Denisovans, and African modern humans diverged more than appeared within large agricultural populations of the Holo- 200,000 y before the transition from Acheulean to MSA in Africa cene. However, genetic evidence suggests that the “epide- began. It is now a stretch to connect any technological innovation miological transition” model does not adequately describe the to Neanderthal and Denisovan origins. Some evidence suggests importance of immunity in prehistory (17). Just as mutational that Acheulean assemblages, characterized by handaxes and load can have strong long-term effects on population growth or other large cutting tools, first entered Europe only around decline, so parasite and pathogen load can impact fertility and 600 ka, a possible coincidence with the earliest Neanderthals susceptibility to environmental stresses. Many adaptive genes (12). However, Acheulean industries of India and Southwest Asia acquired by introgression from Neanderthals and Denisovans have much earlier dates. No known archaeological transition involve immunity. Invasive species sometimes exhibit a “lag” occurred across the plausible Neanderthal-Denisovan range at between their first appearance in a new region and their sub- the time these populations first invaded Eurasia. sequent rapid population growth, during which they may ac- Many biological dimensions affect invasive potential in plants, quire new genes by introgression from resident populations. It insects, and vertebrates, including pathogen relaxation, life is possible that Late Pleistocenemodernhumansfolloweda history traits, ecological tolerances, genetic diversity, and release similar pattern, appearing in Southwest Asia more than of mutational load (13). Looking more broadly at such traits may 100,000yago,buttakingsometimebeforetheydispersed help to explain both Neanderthal-Denisovan population dynam- further into Eurasia. Possibly that time was necessary to acquire ics and modern human invasions. Neanderthal and Denisovan genes modulating immunity to regional pathogens (17). Mutation Load During the portion of their existence sampled by ancient DNA, Life History Traits Neanderthals were subdivided into small populations with little Compared with living great apes, modern humans have short birth genetic exchange (2, 3, 7). Inbreeding within these small intervals, long maturation times, and long life spans. These life populations imbued Neanderthal individuals with a higher history traits reflect tradeoffs that may have influenced the in- fraction of deleterious mutations than living people (14). The vasion potential of hominin populations. Neanderthals and pre- substantial cost of this mutationloadmayexplainthein- dispersal modern humans in the Levant both shared relatively trogression bias against functional regions in the Neanderthal high mortality among young adults, possibly limiting cultural genome into modern human populations. Although Deniso- transmission via older adults and thereby constraining ecological vans are known only from one locality, the high-coverage adaptability (18). Upper Paleolithic Europeans had much lower Denisova genome also indicates a lengthy history of in- young adult mortality, possibly contributing to their population breeding (5). Origins may be a different matter, however. A growth. As in the case of technology, life history evolution is often moderate bottleneck can purge deleterious alleles from a imagined as an evolutionary ratchet, but life history traits may population, facilitating biological invasion in some cases (15). have fluctuated under local or regional selection. Neanderthals Modern humans in Eurasia and Neanderthal-Denisovan an- themselves, sampled relatively late in their existence, had higher cestors may have benefited from their founding bottlenecks, adult survivorship