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Home , Archaic humans, Chris Stringer, Denisovan, Homo erectus, Homo heidelbergensis, Human

Ko J of Biol Res-Thessaloniki (2016) 23:17 DOI 10.1186/s40709-016-0054-7 Journal of Biological Research-Thessaloniki

REVIEW Open Access Hominin interbreeding and the of variation Kwang Hyun Ko*

Abstract confirms the “out of ” theory, but the evidence also supports interbreeding betweenHomo sapiens and other hominins: , , and heidelbergensis. This article explains how inter- breeding between early H. sapiens and archaic hominins occurred. The availability of edible in aided the spread of the unaggressive, highly cooperative Neanderthals, who interbred with H. sapiens in Asia, resulting in a higher admixture of DNA in East Asian . Geographical variation in degree of interbreed- ing between H. sapiens and Neanderthals likely contributed to neurological and behavioral differences in modern . Similarly, with genetic admixture were better able to dwell in mountainous , allow- ing their genetic legacy to cross the Himalayas and persist in Southeast Asian and Oceanian H. sapiens. In the Sub- Saharan , unaffected by Denisovan or Neanderthal interbreeding,H. sapiens interbred with H. heidelbergensis, because high militated against fire-making and allowed the survival of these non-fire-making hominins. Keywords: Neanderthal, Homo sapiens, Denisovan, , Hominin interbreeding

Background to make up a single, continuously gradient (as distinct There are two branching hypotheses on the origin of the from categorically separate) human . human species. The most widely accepted is the “out of DNA analysis demonstrating the of “Mito- Africa” (OOA) theory, which holds that archaic Homo chondrial Eve” has strongly corroborated the recent Afri- sapiens evolved into anatomically modern humans solely can origin model of OOA by providing crucial support to in Africa between 200,000 and 60,000 ago [1]. This the theory that H. sapiens moved from Africa to replace hypothesis further proposes that members of one branch residing hominin populations elsewhere [4]. Mitochon- of H. sapiens left Africa at some point between 125,000 drial Eve is the most recent matrilineal common and 60,000 years ago, and that over a long period, these of all humans currently alive. Women pass along mito- H. sapiens replaced more “primitive” populations of other chondrial DNA unchanged during sexual , hominins in Asia or , such as Homo neandertha- and the DNA of this most recent from whom all lensis and [2]. currently living humans descend through an unbroken The competing theory is the multiregional evolu- line on their ’s side proves that modern humans tion hypothesis [3], which argues that some or all of the only evolved once, most likely in , sometime among contemporary human races is between 150,000 and 200,000 years ago. attributable to genetic from either other H. At the same time, however, studies suggest that Nean- sapiens or from other species. In the derthals, our closest-known evolutionary relatives, coex- multiregional model, all archaic human forms worldwide, isted with H. sapiens on for more than 5000 years such as H. erectus and Neanderthals, as as modern and frequently interbred with modern humans [5]. forms, subsequently evolved together into the diverse According to researchers, at least one-fifth of the Nean- populations of modern H. sapiens, which are considered derthal may lurk within modern humans, influ- encing traits including the appearance of the and people have today and the they get. This *Correspondence: [email protected]; [email protected] Hanyang University, Seoul, South Korea finding indicates that a true “” of Neanderthals

© 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 2 of 9

may not have occurred [6], but that they may have been of Denisovan ancestry in the islands of , particu- absorbed into H. sapiens. Genetic evidence shows that larly , and some parts of mainland other archaic hominins, such as the Denisovans, also Asia, such as Tibet. interbred with H. sapiens [7]. The most current version of the OOA hypothesis emphasizes the African origin Why does Neanderthal ancestry appear to a higher degree of most human populations but allows for the possibil- in Asia? ity of local contributions/interbreeding between humans All H. sapiens living today have interbred to some degree and other hominins [8]. Consequently, this article mainly with Neanderthals, Denisovans, or other hominins, and discusses Neanderthal–human interbreeding, while also as outlined above, we know that these hominin groups explaining other admixtures of with lasted longer and interbred more in some parts of the hominins who were their contemporaries, such as Den- world than in other areas. isovans and H. heidelbergensis. Most hominins other than Denisovans and Neander- thals were simply replaced by H. sapiens that migrated Origin of race: human interbreeding with Neanderthals out of Africa, but sufficient interbreeding occurred with and Denisovans Denisovans and Neanderthals in to leave a sig- Neanderthals are an extinct species of human (in the nificant mark on modern human DNA [15]. Because Homo), related to modern humans [9]. Traces left Neanderthals ranged only from Europe to West Asia, the by Neanderthals include and stone , which question of why there were two waves of interbreeding have been found all over Eurasia, from Western Europe between East Asian H. sapiens and Neanderthals remains to central and northern Asia. Neanderthals are generally a mystery. The answer to this question lies in differences classified by biologists as H. neanderthalensis, and some- in , and in particular aggressiveness, between times as Homo sapiens neanderthalensis. groups of hominins. Denisovans are another extinct species of humans, Homo heidelbergensis, which exhibited proto-Nean- similar to Neanderthals. The Denisova is located derthal traits, existed in Eurasia as early as 350,000– in southwestern , in the Altai near the 600,000 years ago, while the first Neanderthals appeared Russian border with and Mongolia [10]. Research between 200,000 and 250,000 years ago [16]. At varying shows that Denisovans shared a common origin with times, Neanderthals inhabited the region from Western Neanderthals but were genetically distinct. Europe to Central Asia; their eastern and northern range Recent genetic studies have shown a higher Neander- extended to Okladnikov in the Altai region and Byzovaya thal admixture in East Asians compared with Europeans in the Ural region of present-day Russia [17]. Neander- [11], most likely indicating that at least two independent thals started to disappear/interbreed with H. sapiens -flow events must have taken place in early mod- from the time the latter migrated to Europe. find- ern humans and that the early of East Asians ings have indicated brutality and among H. sapi- experienced more admixture than those of Europeans ens living 10,000 years ago [18]. The evidence has shown after the divergence of these two groups [12]; to put it in that in addition to interbreeding, Neanderthals were another way, studies seeking to explain why East Asians also very often killed by H. sapiens, and in related find- inherited 15–30 % more Neanderthal DNA than Euro- ings, genetic studies have shown that the in peans have concluded that East Asians interbred with ADSL, GLDC, and SLITRK1 , which are associated Neanderthals in two waves [13]. with hyperactivity and aggressive behavior in modern The first interbreeding with Neanderthals occurred humans, were not found in Neanderthals [19–21]. Thus, in the Middle East before the ancestors of modern non- by multiple methods, H. sapiens were responsible for the Africans spread out across Eurasia. The ancestors of extinction of Neanderthals, who were more cooperative modern Europeans and Asians then split out of this and less aggressive than H. sapiens according to studies migrant group [12], and the ancestors of East Asians from various fields. interbred again with Neanderthals after the split. The first It should be noted that compared to Africa, Eurasia humans with proto-Neanderthal traits are believed to lacks predators that could have presented a threat to have existed in Eurasia as early as 350,000–600,000 years hominin species. The increase in species richness or bio- ago, with the first “true Neanderthals” appearing between diversity that occurs from the poles to the tropics is often 200,000 and 250,000 years ago. referred to as the latitudinal diversity gradient (LDG), As this implies, Neanderthals and Denisovans were and the greatest is found in the tropics [22]. likely more closely related to one another than either was The African continent lies almost entirely within the to modern humans [14]. Although the range covered by tropics and extends equally to the north and south of the Denisovans is argued, studies have confirmed the impact equator, which creates favorable conditions for , Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 3 of 9

including large predators [23]. The rich vegetation in the Middle East, as mentioned above. Compared with Africa, where edible fruits and nuts are abundant, results Europe, the -abundant regions of East Asia were in a diversity of species, and many , able to support larger populations of hominins. In such such as , lions, vultures, , and chee- an environment, aggressiveness and violence would have tahs, reside exclusively in this biologically diverse region, been more disadvantageous for survival (Fig. 1). where they once posed a major threat to human species. In the Eurasian region, in contrast, where Neanderthals Denisovan interbreeding evolved and ultimately ranged, there were no carnivores Denisovans, which were related more closely to Nean- that regularly preyed on humans. Thus, the Neanderthals derthals than to humans, also interbred with H. sapiens. that ranged in Eurasia evolved toward peaceful behavior. Genetic variation of Denisovans is low compared to that Thus, the H. sapiens that came after H. heidelbergen- of H. sapiens, but Denisovans were present in large parts sis began their journey in East Africa, where they had to of Asia for possibly more than 110,000 years, allowing compete with other , including archaic hominins, H. sapiens in Asia to obtain Denisovan traits from inter- and watch out for dangerous predators. The hyperactivity breeding [7]. and violence of H. sapiens, which distinguish them from Evidence indicates that the highest Denisovan admix- Neanderthals, were an essential part of their survival, ture is found in Oceanian populations, followed by many because they had to fight and often kill predators and Southeast Asian populations, but recent research has competitors. also found indications that parts of mainland Asia, such as Tibet, have small traces of Denisovan DNA [27]. Edible insects and Asia Denisovans were adapted to surviving at high altitudes, Although Neanderthals never inhabited East Asia, East and Denisovan have been found in high in Asians have more Neanderthal DNA than Europeans do. Siberia; researchers have further discovered that Tibetans The peaceful of Neanderthals would have been are inheritors of the ancient Denisovan trait of able advantageous in East Asia due to the large of amount edi- to regulate oxygenation [28]. The highest levels of ble insects available—considerably higher than in Europe. interbreeding with Neanderthals, which were genetically Before a rise in human density forced peo- closer to Denisovans than H. sapiens were, occurred in ple to turn to , hominins were hunter-gath- East Asia, and East Asians show a small, relatively insub- erers, whose mostly consisted of fruits, nuts, and stantial fraction of Denisovan ancestry. Significant levels insects. Prior to the of animals in approxi- of Denisovan genes, however, remain in non-East Asian mately 9000 BCE, hominins would have relied on hunt- populations (Southeast Asians and ) residing ing and scavenging to obtain what they ate. Due far from the in Siberia. to the instability of meat supplies obtained from hunt- Interbreeding with Denisovans significantly affected ing, partly a result of unreliable tools, hominins largely H. sapiens populations on the island of New Guinea, depended on insects for ; from caves where the highest mountains and highlands in Australa- in the and , containing , beetle sia are found. In general, populations that proliferated in larvae, lice, ticks, and mites [24], have evidenced this pre- these ranges would have also spread to nearby historic entomophagy. Similar to other great species regions, leaving remnants of Denisovans throughout that eat insects, then, the evolutionary precursors of H. Asia. At the end of the , the separation of the sapiens were also entomophagous, and staple insects rep- Sahul and Sunda shelves from mainland Asia, caused by resented an important part of their diet. rising sea levels, resulted in the local population of Oce- Prehistoric entomophagy practices have persisted over ania (and parts of ) being less affected by time. Cave in Altamira, North , dating the admixture of Neanderthals with H. sapiens. Thus, from approximately 30,000–9000 BCE, depict the col- traces of Denisovans were more perceptibly preserved in lection of edible insects and wild bee nests, seeming to these regions. suggest an entomophagous . Cocoons of wild silk- worm (Theophila religiosae) found in ruins in the Shanxi Why Neanderthals lost out to Homo sapiens Province of China dateback to 2000–2500 years BCE. Although Neanderthals did interbreed with H. sapiens, The cocoons were discovered with large holes, suggest- the majority of their population went extinct from com- ing that the pupae had been eaten. The eating of insects petition with H. sapiens. As follows from the possession is still observed in the developed of modern-day by H. sapiens of a mutated gene related to , fos- Asia [25]. sil evidence reveals that Neanderthals were killed by H. The ancestors of East Asians interbred with Nean- sapiens in acts of violence [20]. Furthermore, although derthals a second time after the earlier interbreeding in Neanderthals possessed development enabling Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 4 of 9

Fig. 1 Number of edible insect species by country [26]. Source: Centre for geo information, Wageningen University, based on data compiled by Jongema 2012 greater visual acuity than H. sapiens, the latter had bet- states that Westerners look at the focal object more rap- ter -processing abilities [29]. In general, because idly and spend more time looking at it, whereas Chi- Neanderthal were devoted to vision and spa- nese have more saccades, which means that tial memory, this left less area for and they move their eyes more, particularly back and forth interactions. between the object and the background [33]. Furthermore, Neanderthals were less aggressive and Interbreeding and race more “autistic” than H. sapiens. Genes related to hyper- People from East Asian countries have approximately activity and aggression are, in fact, only found in H. sapi- 20 % more Neanderthal DNA than Western Europe- ens. Asians and Pacific Islanders present less symptoms ans, and these differences in levels of interbreeding with linked to hyperactivity and aggressiveness, such as atten- Neanderthals caused certain neurological differences tion deficit hyperactivity disorder (ADHD), and East observed today [16]. Asians score the lowest in terms of aggressive behavior. A recent study conducted by Park & Huang [30] In the United States, both immigrants of East Asian ori- showed evidence of cultural differences between West- gins and mainland Asians show lower crime rates com- erners and East Asians, resting in differences in areas pared with Black and White populations [34]. deep in the brain. Biologically, White American showed increased activation in areas related to language The significance of Homo heidelbergensis and reasoning, such as Wernicke’s and Broca’s areas, Neanderthals, Denisovans, and modern humans (H. sapi- whereas East Asians presented stronger activity in per- ens) are all descended from H. heidelbergensis. Between ceptual regions, such as the visual-premotor association 300,000 and 400,000 years ago, one branch of this group area [31]. Similarly, European brains have to work harder became independent of other hominins; some of this at relative judgment, whereas East Asian brains find group left Africa [35]. One (sub)group branched north- absolute judgments more challenging [32]. In addition, west into Europe and West Asia and eventually evolved adults from Western process information ana- into the Neanderthals, while the other group ventured lytically by focusing on key features, whereas adults from eastward throughout Asia, eventually developing into the East process information in a more holistic manner the Denisovans. The remaining members of this group, [33]. One of the who conducted that study H. heidelbergensis, evolved into H. sapiens approximately Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 5 of 9

130,000 years ago in the dry savannahs in Africa, and Fire‑making and humidity then themselves migrated to other regions and continents The use of fire marked a turning point in human evo- [36]. These humans were more adept at controlling fire lution. The fire drove away predators and insects and than the preceding African hominins had been, but the provided additional warmth to humans. Importantly, humid tropical regions did not foster the development of with fire allowed humans to conserve energy fire-making. Homo sapiens that settled in the tropics of during , because less energy is spent digest- and Africa were genetically influenced by the ing or chewing cooked . One study [40] states that abilities of the anteceding hominins in those regions, who the energetic benefit of consuming cooked foods is very were less dependent on fire-making. high; further, another study [41] found that mice given cooked meat gained 29 % more weight than mice fed raw A short “”—before Homo heidelbergensis meat over a period of 5 weeks, even though the latter Before H. heidelbergensis appeared, H. erectus originated consumed more meat. Furthermore, with the use of fire, in Africa and spread throughout Eurasia, as far as pre- formerly indigestible or toxic components of plants, such sent-day , , , China, and . The as mature , tubers, raw cellulose, thick stems, large H. erectus who remained in Africa is now widely accepted leaves, and seeds, became part of the hominid diet; and as the direct ancestor of all later hominins, including H. hominins saved energy not only on digesting but also on heidelbergensis, H. sapiens, H. neanderthalensis, and the foraging and chewing [40]. Hominid brain increased Asian H. erectus [16]. The group that eventually became steadily overtime, but starting at least a million years ago, H. heidelbergensis in Africa had established populations the rate of increase sped up, a change explained by the in Europe and South Asia by approximately 500,000 years early control of fire exhibited by H. erectus and the sub- ago. sequent nutritive benefits. The current archaeological By approximately 300,000 years ago, regional dif- evidence shows at least million years of widespread fire- ferences began to develop as these H. heidelbergensis making, but the actual beginning of fire-making would adapted to their new environments, having collectively have been much earlier. become independent of other hominins shortly after leaving Africa. At this point, one group became the Conditions for fire‑making Neanderthals, and another group developed into the Fire provides extra calories by making foods easier to Denisovans. The H. heidelbergensis remaining in Africa digest, but fire-making is a difficult task that the earliest evolved into H. sapiens [37]. hominins could not accomplish. One important condi- Homo sapiens eventually spread from Africa into Eura- tion for fire-making is low humidity: if relative humidity sia and replaced the residing hominins; however, a con- (RH) is high, it is hard for moisture to evaporate [42], and siderable degree of interbreeding with archaic hominins at high humidity, will absorb more moisture, making also occurred. Long before the appearance in Eurasia of ignition more difficult. Wild fires occur more frequently H. heidelbergensis and the Neanderthals, the Denisovans, in regions with low humidity, because fuels become drier. and ultimately H. sapiens, the Asian H. erectus inhabited According to the Köppen–Geiger climate classification an overlapping area [38], until it was replaced by those system, some parts of Africa, South America, and Oce- successor species and others. However, H. erectus on the ania are classified as tropical humid, more specifically, mainland went extinct long before the arrival of H. sapi- , tropical savannah, or tropical mon- ens, and so the influence of any admixture of H. erectus soon. This classification takes into account annual and with H. sapiens via Neanderthals and Denisovans would monthly temperatures, precipitation, and seasonality be negligible. of precipitation [43]. In general, the most humid places on Earth are located in the tropics, due to their proxim- Africa and of interbreeding ity to the equator (leading to more sun and warmth) and Homo sapiens interbreeding with Neanderthals or Denis- high precipitation levels. In these regions, fire-making is ovans did not occur in the Sub-Saharan regions, although difficult. the and Yoruba were influenced by a A correlation can be detected between climate zone Neanderthal-influenced Eurasian heritage [39]. Nean- and : native populations in tropic zones have derthals and Denisovans never lived in Sub-Sahara and smaller brains than people from other zones [44]. The never left a genetic mark on Sub-Saharan regions, but link between brain size and is, of course, a interbreeding between Sub-Saharan Africans and an as- controversial issue, and larger brains do not necessarily yet-unknown hominin, such as H. heidelbergensis, has correlate with greater intelligence. However, the develop- been suggested. ment of intelligence derived from fire-making and better Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 6 of 9

nutrition would certainly have been hampered in tropi- Middle East after the introduction of a Eurasian heritage cal areas, where the relative humidity is very high. Thus, [39]. the survival of hominin species in tropical regions would The smaller brain detected in aboriginal popu- have been more difficult given the lack of recourse to lations in the tropical regions of Africa and South Asia fire and resulting benefits, and these people would have can be attributed to interbreeding with H. heidelbergen- depended more on cognitive capacity developed from sis [46]. These humans presumably benefited from inter- foraging and watching out for predators (Fig. 2). breeding with hominin ancestors who depended less on fire and likely had cognitive aptitudes making them more Brain size and interbreeding adept at surviving in the tropics. Homo heidelbergensis mostly had smaller brains than A correlation between IQ and brain size has been Neanderthals, Denisovans, and H. sapiens. While no observed in some studies, but this controversial find- traces of H. sapiens interbreeding with Neanderthals or ing is far from conclusive [47]. The definition of intel- Denisovans have been detected in Sub-Saharan Africa, ligence itself is arguable and IQ as a measure has come as noted, genetic studies show that H. sapiens did inter- under various kinds of criticism; the of the breed with H. heidelbergensis in this region [46]. Brain brain may matter more than the brain size. size differences have been noted among people of Sub- Regardless, and for what it is worth, studies of brain size Saharan African descent, Australian Aboriginals, and based on cranial capacity show lower values in the tropi- people of European descent, the former two of which cal regions of Africa, South Asia, and Oceania, regions showed smaller brains [44]. There are, however, excep- where fire-making would have been difficult, as this -sec tions in Sub-Saharan Africa. Researchers have found tion has discussed (Fig. 3). traces of western Eurasian Neanderthal-associated DNA Furthermore, without an archaic Neanderthal ancestry, in the southern African Khoisan and Yoruba peoples, Sub-Saharan African populations would be more affected who would then have migrated back into Africa from the by genes linked to aggression or hyperactivity, which are

Fig. 2 Köppen climate classification. Tropical/megathermal climates, Af/Am/Aw, high rainfall, hot temperatures [45] Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 7 of 9

Fig. 3 Connection between average cranial capacity and geographic ancestry of H. sapiens [44]

found only in H. sapiens. This finding could help account interbreeding with Neanderthals led to more peaceful for the differences in violence or aggression found in the behavior in humans inheriting Neanderthal genes. Previ- human race today. ous studies have indicated that Neanderthal interbreed- Even so, any implications would not be significant. ing did not Sub-Saharan populations, with the Many cross-cultural exchanges have occurred in the last exception of a few that migrated back from the few 100 years. The states that he Middle East. is unsure whether there is any population that does not To sum up, traces of archaic hominin ancestry have have any Eurasian DNA [39]. The study will only provide been detected in local populations, but the implications information regarding Neanderthal DNA acquired thou- of interbreeding for the modern population should not sands of years ago. be used to justify racial stereotypes. In multicultural , races have mixed to the point that sources Interbreeding and the human race: conclusion of past interbreeding among hominin groups have East Asians have slightly larger brains than Europe- become insignificant. In addition to the countless histori- ans [48]. In more detail, the perceptual brain regions cal migrations that have occurred, H. sapiens themselves are larger in East Asians, whereas the regions related to have continued to evolve separately in different regions, language are larger in Europeans. Sub-Saharan Africans and they are not the same humans that lived 10,000 years mostly have smaller brains than the aforementioned two ago. Nonetheless, many local, isolated aboriginal popu- groups. The significant differences in brain size observed lations in Africa, Eurasia, and Oceania have remained between tropical and other regions were influenced by relatively stable, and their brain sizes show traces of past tropical conditions, which prove harsh for fire-making, interbreeding [48]. a key for accessing the nutrition necessary to grow big brains. Instead, H. sapiens in tropical regions Addendum to the conclusion: interbred with populations that depended less on fire for In addition to H. heidelbergensis, Neanderthals, and Den- survival, leading to smaller brains in these areas. isovans, there is another species of archaic hominin that In terms of hyperactivity and aggression, the lowest should be considered, one with a very small brain that scores among present human populations are obtained lived up until recently (around 10,000 years ago). Homo by East Asians, followed by Europeans and then Sub- floresiensis was a distinct ancient species of hominin Saharan Africans [49]. The genes pertaining to aggres- discovered on , an island in . The most siveness and hyperactivity originate with H. sapiens, and important identifying features of H. floresiensis are its Ko J of Biol Res-Thessaloniki (2016) 23:17 Page 8 of 9

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