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Home , Abrigo do Lagar Velho, Denisova Cave, Orrorin, Scladina

DNA and sapiens

Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

Anthropological Review • Vol. 83(1), 93–107 (2020)

ARNTHROPOLOGICAL EVIEW Available online at: https://content.sciendo.com/anre Journal homepage: www.ptantropologiczne.pl Volume 83, 2020

What have the revelations about Neanderthal DNA revealed about Homo sapiens?

Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

Instituto de Filosofia e Ciências Humanas, Cidade Universitária José da Silveira Netto, Universidade Federal do Pará, Brasil

Abstract: Genetic studies have presented increasing indications about the complexity of the interactions between Homo sapiens, and , during . The results indicate potential replacement or admixture of the groups of hominins that lived in the same region at different times. Re- cently, the time of separation among these hominins in relation to the Last Common Ancestor – LCA has been reasonably well established. Events of mixing with emphasis on the Neanderthal gene flow into H. sapiens outside Africa, Denisovans into H. sapiens ancestors in Oceania and continental Asia, Neanderthals into Denisovans, as well as the origin of some phenotypic features in specific populations such as the color of the skin, eyes, and predisposition to develop certain kinds of diseases have also been found. The current information supports the existence of both replacement and interbreeding events, and indicates the need to revise the two main explanatory models, the Multiregional and the Out-of-Africa hypotheses, about the origin and evolution of H. sapiens and its co-relatives. There is definitely no longer the possibility of justifying only one model over the other. This paper aims to provide a brief review and update on the debate around this issue, considering the advances brought about by the recent genetic as well as morpho- logical traits analyses.

Key words: evolution, admixture, genetics, morphology, Homo sapiens

The growing discoveries about Neander- the human history is much more complex thal and DNA have been rais- than what would have been supported by ing striking new information concerning just one, or another particular model cur- both groups of hominins (Kuhlwilm et al. rently not recognized. However, it might 2016; Sankararaman et al. 2016; Vernot et bring the need for revision and acceptance al. 2016; Roger et al. 2017). According to of assumptions of models, as the Multi- Rogers (2017a, b) and Fernando and Josh- regional Evolution, that was previously ua (2019), the descriptions of the diverse refuted (Manderscheid and Rogers 1996; forms of interactions that existed, have in- Larh and Foley 1998; Stringer 2002; 2012; creasingly allowed the understanding that 2014; 2016; Weaver 2012).

REview Article Received: September 30, 2019; Revised: February 27, 2020; Accepted: February 29, 2020 DOI: 10.2478/anre-2020-0008 © 2020 Polish Anthropological Society 94 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

One of the new data that brings such ideas that considered the unilinear evo- discussion is related to one from lution of several groups of hominins liv- ’s Hohlenstein-Stadel ing spatially separated, but converging to and a jawbone from ’s a single pattern, for ideas focused on a Cave, both dated to 120 ka (Peyrégne single origin of H. sapiens, with their sub- et al. 2019). They have added more in- sequent divergence (Schwartz and Tat- formation about the population history tersall, 2010). However, this change oc- in Neanderthals during the Middle and curred slowly, both due to the theoretical Late Pleistocene. Overall, the results of clashes marked by divergent theoretical the genetic data indicate similarity of the tendencies and the paleoanthropolog- mtDNA (maternal information) of a Ne- ical data which appeared in increasing anderthal girl, dated 90 ka, found in an but slow rhythm (Caspari and Wolpoff, Altai cave, in , to the 120 ka DNA 2013; Trinkaus, 2013). of some Western Europe individuals. In the mid-twentieth century, the par- This finding emphasizes how the pro- adigm shared among many scholars was cess of interbreeding and, potentially, based on the existence of a single hu- replacement, might have been recurrent man species, which would have evolved among several populations of hominins, gradually and sequentially throughout mainly those within the genus Homo Pleistocene, but concomitantly in dif- (Paul et al., 2019). Eventually, such in- ferent places: the so-called “Polycentric formation may come in line to give sup- Evolution Theory” by Franz Weidenre- port to the explanation of our own emer- ich (1947). It is a model by which the gence and expansion of the model called regional sequences were reasoned as an “Out of Africa”, but not only this model. interconnected web evolving in a single This is only one of several examples of common direction. Thus, it would be interactions between Neanderthals and considered a unilinear concept oriented Homo sapiens (Kuhlwilm et al. 2016; San- towards convergence, as previously sug- kararaman et al. 2016; Vernot et al. 2016; gested by Aleš Hrdlička (1927). Roger et al. 2017; Dannemann and Kelso Although Weidenreich’s theory 2017) which put into question the two (1947) was based on assumptions sup- main current models oriented to explain ported by other scientific models, the the emergency and evolution of Homo sa- explanation of orthogenesis as the deter- piens: the Out of Africa and the Multire- mining factor, as outlined by polycentric gional model. A brief revision and update evolution, was rejected by the Modern on the debate around this issue, consid- Synthesis (Huxley 1942), and finally ering the advances brought about by the by Coon’s model (Coon 1962), which recent genetic as well as morphological admitted parallel evolution occurring traits analyses is the goal of this paper. strongly isolated in various regions of The emergence and evolution of Homo the world. This would have several con- sapiens under two different views sequences for the ideas concerning the The explanatory models that deal with formation of distinct biologic groups cre- the origin of H. sapiens, as well as the evo- ated at that time, as well as its refutation. lution of the genus Homo, changed from One of those is the hypothesis for the the 1980s onward (Manzi, 2011). Briefly, evolution of the Presapiens, in particular there has been a gradual substitution of deriving from the discussions related to Neanderthal DNA and Homo sapiens 95 the Fontéchevade cranial remains, linked Evolution and the Out-of-Africa. Wol- to the Swanscombe and Steinheim speci- poff et al. (1980a, b; 1984) proposed the mens (Vallois 1954). In this case, and ac- Multiregional Evolution model, which cording to Howell (1952), Neanderthals was largely based on Weidenreich’s the- and modern would have sepa- ory of polycentric evolution (1947). Ac- rated only during the Eemian Interglacial cording to this perspective, the present period. After this event, the Prenean- human diversity would have been the derthals of Southwest Asia would have result of small and constant changes be- evolved into modern humans, while the tween the populations and within the Preneanderthals of Europe would have species as a whole, occurring from the become the robust classic Neanderthals. original geographic diffusion of the ge- However, this concept was not supported nus Homo (Wolpoff, 1970; Thorne and by subsequent research (Bräuer 2008), Wolpoff 1981; 1992; Wolpoff et al. 1984; in special those that revealed affinities 1994). This model suggests that there of Presapiens with Neanderthals and would have been successive stages and Preneanderthals (Hublin 1985; Hublin / or regional variants within a general- and Tillier 1981, 1992; Trinkaus 1981; ized archaic species – and 1983). In addition, discoveries of some later within H. sapiens (Wolpoff 1980b). hominids, such as the partial skulls of The result was a progression of region- Arago and Biache St. Vaast, demonstrat- al changes that, with the persistence of ed only one lineage in Europe that led a single polymorphic humanity in each to the Neanderthals (Bräuer 1984a, b). geological time period, was evolving into No diachronic tendency of reduction in variants of the modern species (Thorne size could be observed in the Neander- and Wolpoff 1981; Wolpoff 1980a). As a thals of the Near East, and the subse- consequence, the H. sapiens taxon would quent review of dating revealed that early include the existing humanity, but also modern humans and Neanderthals were extinct morphotypes such as Neander- almost contemporaneous in this region thals in Europe and the Near East, as (Trinkaus 1986; 1992; Hublin 1992). well as several in Africa During the 1960s and 1970s, only a and East Asia during the Middle Pleisto- few researchers insisted on the idea of cene, known as “archaic H. sapiens” (Wol- local continuity between modern and an- poff 1986), later called H. heidelbergensis cient populations, and by the late 1970s (Schwartz and Tattersall 2010). Thus, the question of the origin of modern under the same specific name, H. sapiens, humans was once again widely open. each of these morphotypes was assigned Some researchers, such as Milford Wol- to a different subspecies, with the adop- poff (1980a, b), continued to emphasize tion of a trinomial nomenclature – H. sa- evolutionary continuity in Europe and piens neanderthalensis and H. sapiens sapiens elsewhere, while others, such as Howells (Trinkaus 1983, such as supported by (1976), assumed a recent common origin the hypothesis of Homo sapiens sensu lato of modern humans. (Wolpoff et al. 1994). In the early 1980s a new period of This hypothesis was based on the - discussions about Modern Human ori- servation of a certain degree of “regional gins emerged, focusing mainly on two continuity” present in the morphologies alternative models, the Multiregional of archaic and modern populations with- 96 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva in each geographical area, as suggested concealed, being also referred to H. erec- by Frayer and colleagues (1993). This ob- tus (sensu lato ) or to the entity called “ servation, however, was gradually chal- archaic H. sapiens”. lenged (Lahr 1994; Larry and Foley 1998; Bräuer (1982) was the first to propose Waddle 1994; Weaver 2012; Stringer the Out-of-Africa model, initially called 2012; 2014; 2016), mainly because such “Afro-European sapiens” hypothesis, model would not agree with much of the since Europe provides the best evidence genetic data that suggested a “Single Ori- for replacement. This model suggested gin” for all modern humans (Klein, 1995; an origin of modern humans only in Afri- Larh, 1994, 1996; Lahr and Foley, 1998; ca followed by their dispersion into Asia Stewart and Stringer, 2012; Relethford, and Europe, finally replacing the archaic 2001; Underhill et al. 2001; Serre and populations. In this case it is important Pääbo, 2004). This last approach recog- to stress that “Replacement” would be nizes the geographical branching of the assumed in the place of “Interbreeding”, Homo lineage during the Pleistocene and supported by the Multiregional model the existence of regional forms, but, dif- (Bräuer 1984; 1992; 2008). ferently, sustains the continuity up to the The paleoanthropological data pro- present of only one of these branches, vide information able to point to at the one originated in Africa which would least two distinct waves of immigration be the unique source of all current diver- into Europe occurring sequentially, one sity (Stringer and Andrews 1988; String- during the Early Pleistocene, and the oth- er 2006; 2012). Thus, this view, driven er at the beginning of the Middle Pleis- by more ecological rather than behavioral tocene (Manzi, 2011). The first wave is or cultural motifs, associates the earlier documented only in and is related Homo groups to the diffusion and adap- to a dated to 1.2 Ma found in the tation to the diversity of environments, TE9 stratigraphic layer of the “Sierra del many of which not tropical (Manzi 2011). Elefante” (de Castro et al. 2011), and jaw In this case, H. erectus can be seen only fragments found in the TD6 layer of the as a species from the Far East (Java and “Gran Dolina”, dated in more than 780 ), while its African counterparts Ka (de Castro et al. 1997; Carbonell et al. are considered as a distinct species, H. 2008). Initially the traces found in Gran ergaster (Wood 1991). At the same time, Dolina were referred to as other groups were named as distinct spe- (de Castro et al. 1997). However, the ad- cies, or had the old name reconsidered, vancement of research and discovery of such as H. rudolfensis (Wood 1991), H. TE9 led the group of researchers to sug- heidelbergensis (Rightmire 1996), H. ante- gest that there had been more than one cessor (Bermudez de Castro et al. 1997) speciation event, which then led them to H. rhodesiensis (Hublin 2001), H. georgicus rename the TE9 specimen as Homo sp (de (Gabounia et al. 2002). Castro et al., 2011) so as not to consider According to Manzi (2011), although a necessary link of such specimen to H. the identification of all these different antecessor. species clearly implies an overestima- Homo antecessor and H. heidelbergensis tion of interspecific diversity, this gives a would have competed against each oth- clearer and more intelligible meaning to er for the same phylogenetic position the human varieties that were formerly in the current evolutionary trees of the Neanderthal DNA and Homo sapiens 97 genus Homo, seen as provisional alterna- and Schwartz 2000; 2006; Schwartz and tive models of (Manzi Tattersall 2002; 2005). 2011). The H. antecessor is considered For Rightmire (1998, 2008), which by the Spanish researchers (de Castro advocates the “single species” model, et al. 1997) as the species ancestral to there are problems in the definition of an the evolutionary divergence that would African Middle Pleistocene species that is lead to the evolution of Neanderthals in separated from existing European or East Europe and the emergence of H. sapiens Asian lineages, and would have lived in in Africa. Alternatively, H. heidelbergensis the same time interval. In addition, ac- was claimed for this same role by other cording to him, and Smith et al. (2010), authors (Rightmire 1996). In this con- morphological diversity does not nec- text, the “Sima de los Huesos” material essarily indicate multiple species in the is clearly connected to the Neanderthals Middle Pleistocene. However, it is also be and is characterized by a number of fea- possible to demonstrate the existence of tures that later on in the Pleistocene will other relatively small specificities in each become typical of this group (Dean et al. of the groups. These specificities became 1998). Thus, the H. heidelbergensis would more evident since 400 Ka, with the for- acquire a regional European identity in mation of regional morphological differ- continuity with H. neanderthalensis, but ences finally established in 100 Ka, with differently would evolve in a specific Af- H. neanderthalensis in Europe and Central rican lineage that would lead to H. sapiens Asia, modern humans in Africa, H. erectus (Manzi 2011). in Asia and H. florensiensis, in Australasia The identification of such features is (Smith 2010). fundamental to construct a meaning for In general, the chronology, topology, H. sapiens regardless of the model used and phylogenetic dynamics related to to support its origin and evolution, be- the large geographic dispersion of the cause our species exists primordially due archaic human beings ancestors of the the differences recognized in relation to origin of both Neanderthals and mod- the H. neanderthalensis (Schwartz and Tat- ern humans is still unclear (Rightmire tersall 2010; Caspari and Wolpoff 2013). 2008; Hublin 2009; Stringer 2012). Tat- In this case, although virtually all clas- tersall (1986), for example, suggested sical osteometric measurements show from a macroevolutionary perspective some degree of overlap between the two based on “punctuated equilibrium”, that groups, the overall evaluation of shape by the observed morphological variation geometric morphometry demonstrates a within this group could represent mul- clear separation between the craniofa- tiple species. In other words, it would cial anatomy of the two species (Harva- lead to cladogenesis. However, for Smith ti 2007; Lieberman 2011; Harvati et al. (2010), the observed differences do not 2004;). The Neanderthals also show re- mean, even with significant morpholog- markable differences in the post-cranium ical distinctions, that two populations as well as development standards and ob- may become different species, unless a stetric features (Pearson 2000; Ponce de reproductive barrier is established be- León and Zollikofer, 2001; Harvati 2007; tween them. Weaver and Hublin 2009) which support Considering just models oriented to a separation from H. sapiens (Tattersall explain the origin of H. sapiens, and in ac- 98 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva cordance with Smith and Ahern (2013), The Denisovans, as they are called, the “Out-of-Africa” was an influential are an extinct archaic group of hominins, model during the 1980s because genetic previously unknown, related to both Ne- information obtained by methods used anderthals and modern humans (Prüfer at the time supported the morphological et al. 2014). Through the bone remains evidence consistent with a single demo- recovered from the a ge- graphic scenario. Some of the first and nomic sequence was determined (Meyer main works towards this approach were et al. 2014). The complete sample con- presented by Cann, Stoneking and Wil- sists of two upper molars identified as son (1987); Delson (1988), and Stringer Denisovans – D4 and D8, one deciduous and Andrews (1988). In these works, in- tooth – D2 and a finger phalanx –D3, formation from mtDNA was used to sup- three bones of Neanderthal – D9, D5, port a common ancestor originated in Af- D15, one fragment of bone belonged to rica, around 200.000 Ka. Although these hominin hybrid (Neanderthal – Deniso- findings were reinforced by other - stud van) – D11, and other three human frag- ies (Vigilant et al. 1991; Stoneking et al. ments of bones, not able to be fixed in 1992; Nei and Roychoudhury 1993), the any specific group Homo( sp.) – D14, D6 data accumulated after a series of genet- and D16 (Douka et al. 2019). ic investigations along the last decades The Denisovans teeth were estimat- do not indicate the occurrence of only ed to be chronologically located between replacement or interbreeding, but both, 194,4 ka and 51,6 ka, the Neanderthal often at the same time. bones were estimated between 147,3 ka and 90,9 ka, and the bone with mixed ge- Discussion nome – D11, was found to be between 118,1 to 79,3 ka. In the last decade, the improvement of Genetic information indicates that techniques for extracting genetic material there was a separation between Neander- has provided information about the sep- thal and Denisovan populations from the aration as well as interactions of several future modern humans, between 550 and groups of the genus Homo who coexisted 765 Ka. However, analysis of the Deniso- during the Middle and Late Pleistocene van suggests that Neanderthals (Green et al. 2010; Prüfer et at., 2014; and Denisovans diverged between 381 Meyer et al., 2014; Kuhlwilm et al., 2016; and 473 Ka, while Neanderthals diverged Harris and Nielsen, 2016; Vernot, B. et al. from modern humans for at least 430 Ka 2016; Fernando, A. and Joshua, G. 2019). (Prüfer et al. 2014). In one of these studies, the analysis of The evidence for mtDNA indicates isolated sequences of mitochondrial (mt) Denisovans different from both H. ne- DNA from a hominin femur recovered anderthalensis and H. sapiens, but that from excavations occurred between 1994 shared a common ancestor around 1.0 and 1999, in Atapuerca, Spain, revealed a Ma (Kuhlwilm et al. 2016). The origin similarity to mtDNA from another spec- of these three clades corresponds to the imen from the Denisova Cave, located in morphological discontinuity that occurs Altai, in Southeast Siberia, which is ap- in the fossil record before the appearance proximately 4,000 km from Spain (Meyer of H. heidelbergensis. Thirteen mtDNA se- et al. 2014). quences as well as three other consensual Neanderthal DNA and Homo sapiens 99 sequences referring to the fossil of Sima In one of the analyzes, for example, de los Huesos could also provide estima- the Altai for a Neanderthal and tion for age and time of divergence of the a Denisovan specimen were compared Denisovans. The dates for the Sima de with the sequences of chromosome 21 los Huesos range from 150 to 640 of a Neanderthal from Spain and another Ka, with one-point estimates of about from (Kuhlwilm et al. 2016). The 400 Ka, while the time of divergence be- results indicated that an early divergent tween these hominins and that of Den- population of modern humans in Africa isova ranges from 400 to 1.060 Ka, with also contributed genetically to the Nean- estimates in about 700 Ka (Meyer et al. derthal ancestors, about 100 Ka. How- 2014; Prüfer et al. 2014). ever, the Neanderthal group in question Despite the separation of the two was located in the mountains of Altai. In groups, there was also the opposite ef- contrast, this genetic contribution was fect, that is, a mixture between archaic not detected, either in Denisovan or in and modern human populations, which the two European Neanderthals. Thus, it mainly resulted in specific Neanderthal was concluded that the ancestors of the DNA loci inclusions into H. sapiens (San- Neanderthals of the and kararaman et al. 2014; Vernot and Akey modern humans met and crossed, possi- 2014; Racimo et al. 2015; Fu et al. 2016; bly in the Near East, many thousands of Harris and Nielsen 2016; Gittelman et al. years earlier than reported in other sur- 2016; Simonti et al. 2016; Dannemann veys (Sankararaman et al. 2012). and Kelso 2017; Dannemann et al. 2017). The case of “Lapedo Boy”, found in One of the first studies in this direction the Lagar Velho Shelter, (Zilhão pointed out that Neanderthals shared and Trinkaus, 2002; Almeida et al. 2007; more genetic variants with present-day Zilhão et al. 2007) as well as the Oase 1 humans in Eurasia than with present-day and 2 found in Peştera cu Oase, Roma- humans in sub-Saharan Africa, indicat- nia (Crevecoeur et al. 2009), contrast the ing that the separation occurred before ideas used to support an absolute divi- the divergence of Eurasian groups from sion between H. sapiens and H. neander- each other (Green et al. 2010). Further thalensis (Schwartz and Tattersall 2010). information is also progressively being At first, based only on comparative revealed, such as the Neanderthal gene morphology and anatomical evolution flow into modern humans outside Af- studies the two cases were admitted as rica, Denisovan gene flow into Modern examples of hybridity between the two Human ancestors in Oceania and conti- groups (Rougler et al. 2007; Zilhão et nental Asia (Meyer et al. 2012; Sankar- al. 2007). However, subsequent analyzes araman et al. 2016, Vernot et al., 2016), based on genetic material extracted from Neanderthal gene flow into Denisovans the Oase skeleton finally confirmed- hy (Rogers et al. 2017), and possibly the bridization, with 6 to 9% of Neanderthal gene flow of an unknown archaic group genomic material, and more important- that diverged from other strains more ly, this information corroborated the than one million years ago into Deniso- hypothesis based on the morphological vans (Sankararaman et al. 2014; Mondal analysis (Rougier et al. 2007; Zilhão et et al. 2019). al. 2007; Fu et al. 2015). Nevertheless, for some researchers such cases indicate 100 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva the rarity with which the interactions 1994, 1996; Lieberman, 1995; Stock and with offspring between the two groups Lahr, 2007; Li et al., 2017). The other must have occurred, since only about 4% criticism, based on the fossil record in- of Neanderthal DNA has been identified dicated that the Homo genus in the Pleis- in modern Europeans DNA (Meyer et al., tocene would have different and not con- 2014; Prüfer et al., 2014; Kuhlwilm et al., vergent evolutionary trajectories in the 2016). various regions of the planet (Stringer In general, there are examples in 2002). That is, would be consistent with which the importance of the “Out of Af- a regional differentiation rather than a rica” hypothesis is assigned in order to single modernization trajectory. understand the emergence and evolution Now, the new data coming from ge- of H. sapiens, as what is the case intro- netic material point out that in fact there duced in this paper, which broach and were many moments of interbreeding event of replacement (Wei-Haas 2019). between different hominin groups, ex- Nevertheless, most of the research in isting since the Middle Pleistocene. It human paleogenetic developed since allows reconsidering the Multiregional the beginning of the 21st century reiter- Model, even though works dealing with ate the importance of interbreeding and the morphological character show sub- hybridization (Green et al. 2010; Meyer stantial differences between Neander- et al. 2014; Prüfer et at. 2014; Sankarara- thals and ourselves (Harvati 2003; 2015; man et al. 2014; Vernot and Akey 2014; Harvati et al., 2004; Schwartz and Tatter- Racimo et al. 2015; Fu et al. 2016; Git- sall 2002; 2005; Tattersall and Schwartz telman et al. 2016; Harris and Nielsen 2000; 2006; Tattersall 2007). Such dif- 2016; Kuhlwilm et al. 2016; Simonti et ferences may not have been a great ob- al. 2016; Vernot et al. 2016; Dannemann stacle for the genetic exchange between and Kelso 2017; Dannemann et al. 2017; the several co-contemporaneous groups Fernando and Joshua 2019). These find- and, consequently, hybridization, even ings bring back the importance of the considering the low incidence of this oc- Multiregional Model as another potential currence (Prüfer et at. 2014; Meyer et al. explanation for the origin of H. sapiens. 2014; Kuhlwilm et al. 2016). The bases of the Multiregional Mod- In the case of the Neanderthals and el were widely criticized (Manderscheid H. sapiens, once they met, there may have and Rogers 1996; Larh and Foley 1998; been cases of violence, xenophobia, as Weaver 2012; Stringer 2012; 2014), well as ontogenetic, morphological and mainly due to discontinuity in the fossil behavioral differences that might have record outside Africa, and also as relat- affected the recognition of sexual part- ed to the incompatibilities in the gene ners and the behavioral systems related flow needed to explain the evolution of to mating and, consequently, to the re- Modern Man proposed by such a model. production, as reported in chimpanzees In this case, there was resistance to the and bonobos (Overmann and Coolidge ideas used for indicating the existence 2013). However, the genetic data show of morphological traits as evidence of that this was not always the case. archaic and modern continuity in China According to Groves (2007), repro- and (Groves, 1989; Habgood, ductive isolation may or may not be the 1989; 1992; Larh and Foley, 1994; Lahr, result of speciation. And, species that Neanderthal DNA and Homo sapiens 101 hybridize are not necessarily close rel- African population that had completely atives of one another. This would be in replaced other archaic human species on agreement with several cases of hybrid- their way out of the continent (d’Errico ization between distinct species, such and Stringer 2011). There is increasing as caudate amphibians – Triturus cristatus genetic evidence of cases of interbreed- and Triturus marmoratus – characteristic of ing between H. sapiens, Neanderthals and flat and open meadow regions of Europe Denisovans, what is directly consistent (Arntzen and Wallis 1991). In this case with the Multiregional Model. hybridization occurs, probably unidirec- Perhaps it is time to elaborate a dif- tionally, since all the hybrids possess ferent explanation that encompasses the mtDNA of T. cristatus. However, there is several events regarding the evolution of evidence that some genes would have en- hominin groups since the Middle Pleisto- tered the “pure” species on both sides, cene to the present. However, this does with exchanges occurring at the time of not mean that is necessary to create yet hybridization (Arntzen and Wallis 1991). another Model. Maybe it is time to rec- In there are also several cases of oncile the ones already existing, to find hybridization (Arnold and Meyer 2006), a common explanation that support this reported among New World Monkeys, as so vast horizon of possibilities that is identified in Saimiri species (Carneiro et Humanity. al. 2016; Mourthe et al. 2019) as well as in Old World Monkeys, as Pan troglodytes Authors’ contributions and Pan paniscus (Vervaecke and Elsacker 1992; de Manuel et al. 2016). SG has developed the discussion present- Whatever the forms of interaction that ed and the main structure for the paper; have impacted in the origin and diversity HPS collaborated in terms of revision, of current human populations, one must correction and adaptation of sentences be cautious in the search for specific ap- and ideas in order to clarify its compre- proaches that support circumstantially hension. better explanations concerning those interactions to the exclusion of others. Conflict of interest The human history gradually uncovered by genetic evidence has shown how com- The authors declare that there is no con- plex must have been these interactions, flict of interest regarding the publication and how the extreme models of explana- of this article. tions are unable to correctly describe the magnitude of the evolution of H. sapiens Corresponding author and its co-relatives. As assumed by Sjö- din et al. (2012) it is now recognized that Santiago Wolnei Ferreira Guimarães, In- a phylogenetic origin of modern humans stituto de Filosofia e Ciências Humanas, cannot be more supported by and Afri- Cidade Universitária José da Silveira Net- can only origin. In addition, the events to, Universidade Federal do Pará, R. Au- of interbreeding between Neanderthals gusto Corrêa, 01 – Campus Universitário and modern populations refutes models do Guamá, 66075-900, Belém, Pará-Bra- in which all living humans would recall zill their ancestry to a restricted and small e-mail: [email protected] 102 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

References Cann R, Mark S, Allan W. 1987. Mitochon- drial DNA and human evolution. Almeida F, Alves N, Ponce De León M, Pier- 325(6099):31–6. son B, Duarte C, Bártolo P, et al. 2007. The Carbonell E, De Castro J, Parés J, Pérez- Lapedo Child Reborn: Contributions of González A, Cuenca-Bescós G, Ollé A, et CT Scanning and Rapid Prototyping for an al. 2008. The first hominin of Europe. Na- Upper Infant Burial and Face ture 452(7186):465–69. Reconstruction. The Case of Lagar Velho Carneiro J, Rodrigues-Filho L, Schneider H, Interpretation Centre, Leiria, Portugal. In: Sampaio I. 2016. Molecular data highlight D Arnold, F Iccolucci and A Chalmers, ed- hybridization in squirrel monkeys (Saim- itors. The 8th International Symposium in iri, Cebidae). Genet Mol Biol 39(4):539– Virtual Reality, and Cultural 546. Heritage Vast. Short and Project Papers Caspari R, Wolpoff M. 2013. The process of from VAST. 69–73. Modern Human Origins: the evolution- Arnold M, Meyer A. 2006. Hybridization in ary and demographic changes giving rise primates: one evolutionary mechanism. to modern humans. FH. Smith, J Ahern, Zool 109(4):261–76. editors. The Origins of Modern – Biology Arntzen J, Wallis G. 1991. Restricted gene Reconsidered – Chapter 11. New , flow in a moving hybrid zone of the newts John Wiley & Sons. 355–91. Triturus cristatus and T. marmoratus in west- Coon C. 1962. The Origin of Races. New ern . Evolution 45:805–26. York, Knopf. Bons P, Bauer C, Bocherens H, De Riese T, Cortés-Ortiz L, Jr. T, Canales-Espinosa D, Drucker D, Francken M, et al. 2019. Out García-Orduña F, Rodríguez-Luna E, of Africa by spontaneous migration waves. Bermingham E. 2007. Hybridization in PLoS ONE 14(4):1–25. large-bodied New World primates. Genet- Bräuer G. 1982. Current problems and re- ics 176: 2421–25. search on the origin of Homo sapiens in Af- Crevecoeur I, Rougier H, Grine F, Froment A. rica. Humanbiol Budapest 9:69–78. 2009. Modern Human cranial diversity in Bräuer G. 1984a. A craniological approach to the Late Pleistocene of Africa and Eurasia: the origin of anatomically modern Homo evidence from Nazlet Khater, Peştera cu sapiens in Africa and implications for the Oase, and Hofmeyr. Am J Phys Anthropol appearance of modern Europeans. In: FH 140:347–58. Smith, F Spencer, editors. The Origins of D’errico F, Stringer C. 2011. Evolution, revo- Modern Humans. A World Survey of the lution or saltation scenario for the emer- Fossil Evidence. Liss, New York. 327–410. gence of modern cultures. Philos Trans Bräuer G. 1984b. The “Afro-European sapi- Royal Soc B 366(1567):1060–69. ens-hypothesis” and hominid evolution in Dannemann M, Kelso J. 2017. The contribu- East Asia during the Late Middle and Up- tion of neanderthals to phenotypic varia- per Pleistocene. Cour Forsch Inst Senck- tion in modern humans. Am J Hum Genet enberg 69:145–65. 101(4):578–89. Bräuer G. 1992. Africa’s place in the evolution Dannemann M, Prüfer K, Kelso J. 2017. Func- of Homo sapiens. In: G Brauer, FH Smith, tional implications of intro- editors. Continuity or Replacement: Con- gression in modern humans. Genome Biol troversies in Homo sapiens Evolution. 18:61. Rotterdam, Balkema. 83–98. De Castro Jm, Arsuaga J, Carbonell E, Ro- Bräuer G. 2008. The origin of modern anat- sas A, Martínez I, Mosquera M. 1997. A omy: by speciation or intraspecific evolu- hominid from the lower Pleistocene of At- tion? Evol. Anthropol 17:22–37. apuerca, Spain: possible ancestor to Nean- Neanderthal DNA and Homo sapiens 103

dertals and modern humans. Science 276 burgh, Edinburgh University Press. 274– (5317):1392–95. 85. De Castro Jm, Martinón-Torres M, Gó- Groves C. 2007. Species concepts and specia- mez-Robles A, Prado-Simón L, Martín- tion: facts and fantasies. In: W Henke, I Francés L, Lapresa M, and others. 2011. Tattersall, editors. Handbook of Paleoan- Early Pleistocene human from thropology. Springer. 1861–79. Sima del Elefante (TE) cave site in Sierra Habgood P. 1989. The origin of anatomical- de Atapuerca (Spain): a comparative mor- ly-modern-humans in Australia. In: P phological study. J Hum Evol 61:1–11. Mellars, C Stringer, editors. The human De Manuel M, Kuhlwilm M, Frandsen P, Sousa revolution: behavioural and biological V, Desai T, Prado-Martinez J, et al. 2016. perspectives on the origins of modern Chimpanzee genomic diversity reveals humans. Princeton, Princeton University ancient admixture with bonobos. Science Press. 245–74. 354(6311):477–81. Habgood P. 1992. The origin of anatomically Dean D, Hublin JJ, Holloway R, Ziegler R. modern humans in East Asia. In: G Bräuer, 1998. On the phylogenetic position of the FH Smith, editors. Continuity or replace- pre-Neandertal specimen from Reilingen, ment: controversies in Homo sapiens evo- Germany. J Hum Evol 34(5):485–508. lution. Rotterdam, Balkema. 273–88. Delson E. 1988. One source not many. Nature Harris K, Nielsen R. 2016. The genetic cost 332:206. of Neanderthal . Genetics Fernando A, Joshua G. 2019. Multiple epi- 203:881–91. sodes of interbreeding between Neander- Harvati K. 2003. The Neanderthal taxonomic thal and Modern humans. Nat ecol Evol position models of intra- and inter-spe- 3:39–44. cific craniofacial variation. J Hum Evol Frayer D, Wolpoff M, Pope G. 1993. Theories 44:107–32. of modern human origins: the paleonto- Harvati K. 2015. Neanderthals and their con- logical test. Am Anthropol 95:14–50. temporaries. In: W Henke, I Tattersall, Fu Q, Posth C, Hajdinjak M, Petr M, Mal- editors. Handbook of , lick S, Fernandes D, et al. 2016. The ge- 2nd Edition. Springer. 2243–79. netic history of Ice Age Europe. Nature Harvati K, Frost S, McNulty K. 2004. Nean- 534(7606):200–05. derthal reconsidered: implica- Gabounia L, De Lumley M, Vekua A, Lordki- tions of 3D models of intra and panidze D, De Lumley H. 2002. Décou- interspecific differences. Proc Natl Acad verte d’un nouvel hominidé à Dmanisi Sci U.S.A 101(5):1147–52. (Transcaucasie, Geórgie). Comptes Ren- Howell F. 1952. Pleistocene glacial ecology dus Palevol 1(4):243–53. and the evolution of “classic Neanderthal” Gittelman R, Schraiber J, Vernot B, Mikace- man. Southwest J Anthropol 8:377–410. nic C, Wurfel M, Akey J. 2016. Archaic Howells W. 1975. Neanderthal man: facts and hominin admixture facilitated adaptation figures. In: RH Tuttle, editor. Paleoanthro- to out-of-Africa environments. Curr Biol pology: Morphology and Paleoecology. 26:3375–82. The Hague: Mouton. 389–407. Green R, Krause J, Briggs A, Maricic T, Sten- Howells W. 1976. Explaining modern man: zel U, Kircher M, et al. 2010. A draft se- evolutionists versus migrationists. J Hum quence of the Neandertal genome. Science Evol 5:577–96. 328:710–22. Hublin J. 1985. Human fossils from the North Groves C. 1989. A regional approach to the African Middle Pleistocene and the origin problem of the origin of modern humans of Homo sapiens. In: E Delson, editor. An- in Australasia. In: P Mellars, C Stringer, cestors: The Hard Evidence. New York, editors. The Human Revolution. Edin- Liss. 282–88. 104 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

Hublin J. 1992. in Lahr M, Foley R. 1998. Towards a theory of northwestern Africa. Philos Trans Royal modern human origins: geography, de- Soc B 337(1280):185–92. mography, and diversity in recent human Hublin J. 2001. Northwestern Africa and Mid- evolution. Yearb Phys Anthropol 41:137– dle Pleistocene hominids and their bear- 76. ing on the emergence of Homo sapiens. In: Lieberman D. 1995. Testing hypotheses about L Barham, K Robson-Brown, editors. Hu- recent human evolution from skulls. Curr man Roots: Africa and Asia in the Middle Anthropol 36: 159–97. Pleistocene. Bristol, CHERUB, Western Lieberman D. 2011. The evolution of the hu- Academic and Specialist Press. 99–121. man head. Belknap Press of Harvard Uni- Hublin J. 2009. The Origin of Neandertals. versity Press. Proc Natl Acad Sci U.S.A 106(38):16022– Li ZY, Wu XJ, Zhou LP, Liu W, Gao X, Nian 27. XM, and others. 2017. Late Pleistocene Hublin J, Tillier A. 1981. The ju- archaic human crania from Xuchang, venile mandible from Irhoud (): a China. Science 355:969–72. phylogenetic interpretation. In: C String- Manderscheid E, Rogers A. 1996. Genetic er, editor. Aspects of Human Evolution. admixture in the Later Pleistocene. Am J London. Taylor and Francis. 167–85. Phys Anthropol 100:1–5. Hublin J, Tillier A. 1992. L’Homo sapiens en Manzi G. 2011. Before the emergence of Homo Europe occidentale: gradualisme et rup- sapiens: overview on the Early-to-Middle ture. JJ Hublin, AM Tillier, editors. Aux Pleistocene fossil record (with a proposal Origines d’Homo sapiens. Paris, Presses about at the subspe- Universitaires de France. 291–327. cific level). Int J Evol Biol, Review- Arti Huxley J. 2010. [1942] Evolution: The Mod- cle:1–12. ern Synthesis. M Pigliucci, GB Müller. Meyer M, Kircher M, Gansauge M, Li H, Raci- Cambridge, MIT Press. mo F, Mallick S, et al. 2012. A high-cov- Douka K, Slon V, Jacobs Z, Ramsey C, Shun- erage genome sequence from an archaic kov M, Derevianko A, et al. 2019. Age es- Denisovan individual. Science 338:222–6. timates for hominin fossils and the onset Meyer M, Fu Q, Aximu-Petri A, Glocke I, of the at Denisova Cave. Nickel B, Arsuaga JL, et al. 2014. A mi- Nature 565(7741): 640–3. tochondrial genome sequence of a homi- Klein R. 1995. Anatomy, behaviour and mod- nin from Sima de los Huesos. Nature ern human origins. J World Prehist 9:167– 505(7483):403–18. 98. Mondal M, Bertranpetit J, Lao O. 2019. Ap- Kuhlwilm M, Gronau I, Hubisz M, De Filip- proximate Bayesian computation with po C, Prado-Martinez J, Kircher M, et al. deep learning supports a third archaic in- 2016. Ancient gene flow from early mod- trogression in Asia and Oceania. Nature ern humans into Eastern Neanderthals. Communications 10:246. Nature 530(7591): 429–33. Mourthe I, Trindade R, Aguiar L, Trigo T, Bic- Lahr M. 1994. The Multiregional Model of ca-Marques J, Bonatto S. 2019. Hybridiza- modern human origins: a reassessment tion between neotropical primates with of its morphological basis. J Hum Evol contrasting sexual dichromatism. Int J 26:23–56. Primatol 40(1):99–113. Lahr M. 1996. The Evolution of Modern Hu- Nei M, Roychoudhury A. 1993. Evolutionary man Diversity. Cambridge, Cambridge relationships of human populations on a University Press. global scale. Mol Biol Evol 10: 927–43. Lahr M, Foley R. 1994. Multiple dispersals Pearson O, Grine F, Barham L, Stringer C. and modern human origins. Evol An- 2000. Human postcranial remains from thropol 3:48–60. the Middle and Later of Mumb- Neanderthal DNA and Homo sapiens 105

wa . L Barham, editor. The Middle Sankararaman S, Patterson N, Li H, Päabo S, Stone Age of , South Central Afri- Reich D. 2012. The data of interbreeding ca. Bristol, Western Academic & Special- between Neanderthals and Modern Hu- ist Press. 149–64. mans. PLoS Genetics 8(10):1–9. Peyrégne S, Slon V, Mafessoni F, de Filippo C, Sankararaman S, Mallick S, Dannemann M, Hajdinjak M, Nageli S and others. 2019. Prüfer K, Kelso J, Pääbo S et al. 2014: Nuclear DNA from two early Neandertals The genomic landscape of Neanderthal reveals 80,000 years of genetic continuity ancestry in present-day humans. Nature in Europe. Sci. Adv. 5: eaaw5873. 507(7492):354–7. Ponce De León M, Zollikofer C.P. 2001. Ne- Sankararaman S, Mallick S, Patterson N, Re- anderthal cranial ontogeny and its impli- ich D. 2016. The Combined Landscape of cations for late hominid diversity. Nature Denisovan and Neanderthal Ancestry in 412(6846):534–8. Present-Day Humans. Curr Biol 26:1241– Prüfer K, Racimo F, Patterson N, Jay F, San- 7. kararaman S, Sawyer S, et al. 2014. The Schwartz J, Tattersall I. 2002 Bodo and the complete genome sequence of a Nean- concept of Homo heidelbergensis. H Seidler, derthal from the Altai Mountains. Nature K Begashaw, editors. 25 years of Bodo, 505(7481):43–54. Proceedings of the 4th Phillip V Tobias Racimo F, Sankararaman S, Nielsen R, Huer- Lecture on Human Evolution. Addis Aba- ta-Sánchez E. 2015. Evidence for archaic ba: National Museum 107–27. adaptive introgression in humans. Nat Schwartz J, Tattersall I. 2005. The Human Rev Genet 16:359–71. Fossil Record, Craniodental Morphology Relethford J. 2001. Genetics and the search of Early Hominids (Genera Australopithe- for modern human origins. New York, Wi- cus, , Orrorin) and Overview ley-Liss. (Volume 4). New York, Wiley Liss. Rightmire GP. 1996. The human cranium Schwartz J, Tattersall I. 2010 Fossil evidence from Bodo, Ethiopia: evidence for specia- for the origin of Homo sapiens. Yearb Phys tion in the Middle Pleistocene? J. Hum Anthropol 53:94–121. Evol 31(1):21–39. Serre D, Pääbo S. 2004. Evidence for gradi- Rightmire GP. 1998. Human evolution in the ents of human genetic diversity with- Middle Pleistocene: the role of Homo hei- in and among continents. Genome Res delbergensis. Evol Anthropol 6(6):218–27. 14:1679–85. Rightmire GP. 2008. Homo in the middle pleis- Simonti C, Vernot B, Bastarache L, Botting- tocene: hypodigms, variation, and species er E, Carrell D, Chisholm R, and others. recognition. Evol Anthropol 17(1):8–21. 2016. The phenotypic legacy of admixture Rogers A, Bohlender R, Huff C. 2017a. Early between modern humans and Neander- history of Neanderthals and Denisovans. tals. Science 351:737–741. Proc Natl Acad Sci U.S.A 114(37):9859– Sjödin P, Sjöstrand A, Jakobsson M, Blum M. 63. 2012. Resequencing data provide no ev- Rogers A, Bohlender RJ, Huff C. 2017b. Reply idence for a human bottleneck in Africa to Mafessoni and Prüfer: Inferences with during the penultimate glacial period. Mol and without singleton site patterns. Proc Biol Evol 29(7):1851–60. Natl Acad Sci U.S.A 114(48):E10258–60. Smith F. 2010. Species, populations, and as- Rougier H, Milota S, Rodrigo R, Gherase M, similation in later human evolution. In: Sarcina L, Moldovan O. And others. 2007. CS Larsen editor. A Companion to Biolog- Peştera cu Oase 2 and the cranial mor- ical Anthropology. Oxford: Wiley-Black- phology of early modern Europeans. Proc well. 357–78. Natl Acad Sci U.S.A 104(04):1165–70. Smith F, Ahern J. 2013. Introduction: thoughts on Modern Humans origins: from 1984 106 Santiago Wolnei Ferreira Guimarães, Hilton P. Silva

to 2012. In: FH Smith, C Ahern, editors. Tattersall I, Schwartz J. 2000. Extict Humans. The Origins of Modern Humans, Biology Boulder, Westview Press CO. Reconsidered. New Jersey, John Wiley & Tattersall I, Schwartz J. 2006. The distinctive- Sons. XI–XXV. ness and systematic context of Homo nean- Smith T, Tafforeau P, Reid D, Grün R, Eggisn derthalensis. In: K Harvati, T Harrison, ed- S, Boutakiout M. et al. 2007. Earliest ev- itors. Neanderthals Revisited. New York, idence of modern human life history in Springer. 9–22. North African early Homo sapiens. Proc Thorne A, Wolpoff M. 1981. Regional conti- Natl Acad Sci U.S.A 104(15):6128–33. nuity in Australasian Pleistocene hominid Stewart J, Stringer C. 2012. Human evolution evolution. Am J Phys Anthropol 55:337– out of Africa: the role of refugia and cli- 49. mate change. Science 335:1317–21. Thorne A, Wolpoff M. 1992. The multiregion- Stock J, Lahr M, Kulatilake S. 2007. Cranial al evolution of humans. Sci Am 266:76– diversity in South Asia relative to modern 83. human dispersals and global patterns of Trinkaus E. 1981. Neanderthal limb propor- human variation. In: MD Petraglia, B All- tions and cold adaptation. C Stringer, edi- chin, editors. The Evolution and Histo- tor. Aspects of Human Evolution. London, ry of Human Populations in South Asia. Taylor & Francis 187–224. Springer 245–68. Trinkaus E. 1983. The Shanidar Neandertals. Stoneking M, Sherry ST, Redd AJ, Vigilant L. New York, Academic. 1992. New approaches to dating suggest a Trinkaus E. 1986. The Neandertals and mod- recent age for the human mtDNA ances- ern human origins. Annu Rev Anthropol tor. Philos Trans Royal Soc B 337:167–76. 15:193–218. Stringer C, Andrews P. 1988. Genetic and fos- Trinkaus E. 1992. Morphological contrasts sil evidence for the origin of modern hu- between the Near Eastern Qafzeh-Skhūl mans. Science 239:1263–8. and late archaic human samples: grounds Stringer C. 2002. Modern human origins: for a behavioral difference? In: T Akazawa, progress and prospects. Philos Trans Roy- K Aoki, T Kimura, editors. The Evolution al Soc B 357(1420):563–79. and Dispersal of Modern Humans in Asia. Stringer C. 2006. The origins of modern hu- Tokyo, Hokusen-Sha Publishers 277–94. mans 1984–2004. In: H Soodyall, editor. Underhill P, Passarino G, Lin A, Shen P, Foley The of Africa. Johannesburg, R, Lahr M. 2001. The phylogeography of Jonathan Ball 10–20. Y chromosome binary haplotypes and the Stringer C. 2012. The status of Homo heidel- origins of modern human populations. bergensis (Schoetensack 1908). Evol An- Ann Hum Genet 65:43–62. thropol 21:101–7. Vallois H. 1954. Neanderthals and presapi- Stringer C. 2014. Why we are not all mul- ens. J Royal Anthropol Inst 84:11–30. tiregionalists now. Trends Ecol Evolut Vernot B, Akey J. 2014. Resurrecting surviv- 29:248–51. ing Neandertal lineages from modern hu- Stringer C. 2016. The origin and evolution man genomes. Science 343:1017–21. of Homo sapiens. Philos Trans Royal Soc B Vernot B, Tucci S, Kelso J, Schraiber J, Wolf A, 371(1698):1–12. Gittelman R, et al. 2016. Excavating Ne- Tattersall I. 1986. Species recognition in hu- andertal and Denisovan DNA from the ge- man . J. Hum Evol 15:165– nomes of Melanesian individuals. Science 75. 352:235–9. Tattersall I. 2007. Neanderthals, Homo sapi- Vervaecke H, Elsacker V. 1992. Hybrids ens, and the question of species in paleo- between common chimpanzees (Pan anthropology. Journal of Anthropological troglodytes) and pygmy chimpanzees Species 85:139–46. Neanderthal DNA and Homo sapiens 107

(Pan paniscus) in captivity. Mammalia out a definable difference. V.V. Novotný, 56(4):667–9. A. Mizerová (Eds.): Fossil Man: New Vigilant L, Stoneking M, Harpending H, Facts, New Ideas, Papers in Honor of Jan Hawkes K, Wilson A. 1991. African popu- Jelínek’s Life Anniversary. Anthropos (Br- lations and the evolution of human mito- no) 23:41–53. chondrial DNA. Science 253:1503–8. Wolpoff M, Thorne A, Smith F, Frayer D, Weaver T. 2012: Did a discrete event 200.000– Pope G. 1994. Multiregional evolution: a 100.000 years ago produce modern hu- worldwide source for modern human pop- mans? J Hum Evol 63:121–6. ulations. M Nitecki, D Nitecki, editors. Weaver T, Hublin JJ. 2009. Neandertal birth Origins of anatomically modern humans. canal shape and the evolution of human New York, Plenum. 175–99. childbirth. Proc Natl Acad Sci U.S.A 106 Wolpoff M, Hawks J, Frayer D, Hunley K. (20): 8151–8156. 2001. Modern human ancestry at the pe- Wei-Haas M. 2019. Ancient DNA reveals new ripheries: a test of the replacement theory. twists in Neanderthal migration: genetc Science 291:293–7. surprises pulled from 120.000-year-old Wood B. 1991. Koobi Fora Research Project, bones showcase the nuanced history of Volume 4: Hominid Cranial Remains. Ox- this close human relative. Nature-Sci- ford, Clarendon Press. ence & Innovation. Retrieved from: Zilhão J, Trinkaus E. 2002. A brief history. In: https://www.nationalgeographic.com/ J Zilhão, E Trinkaus, editors. Portrait of science/2019/06/neanderthals-spread- the artist as a child: the gravettian human across-europe-asia-gets-new-twist-from- skeleton from the ancient-dna/ and its archaeological context. Ministério Weidenreich F. 1947. Fact and speculations da Cultura: Instituto Português de Arque- concerning the origin of Homo sapiens. ologia. 13–27. Am Anthropol 49:39–48. Zilhão J, Constantin S, Danciu A, Rodrigo R, Wolpoff M. 1980a. Paleoanthropology. New Trinkaus E, Gherase M, et al. 2007. The York, Knopf. Peştera cu Oase people, Europe’s earliest Wolpoff M. 1980b. Cranial remains of Middle modern humans. In. P Mellars, K Boyle, O Pleistocene European Hominids. J Hum Bar-Yosef, C Stringer, editors. Rethinking Evol 9(5):339–58. the Human Revolution. Cambridge Mc- Wolpoff M. 1986. Describing anatomically Donald Institute for Archaeological Re- modern Homo sapiens: a distinction with- search. 249–62.