Neandertal-Homo Sapiens Reproductive Isolation and the Archaeological and Fossil Records

doi 10.4436/JASS.91021 JASs Invited Reviews Journal of Anthropological Sciences Vol. 91 (2013), pp. 91-110

Human species and mating systems: Neandertal-Homo sapiens reproductive isolation and the archaeological and fossil records

Karenleigh A. Overmann & Frederick L. Coolidge

Psychology Department, University of Colorado, 1420 Austin Bluffs Parkway, Colorado Springs, CO 80918, USA e-mail: [email protected]

Summary - The present paper examined the assumption of strong reproductive isolation (RI) between Homo neanderthalensis and Homo sapiens, as well as the question of what form it might have taken, using insights from the parallel case of chimpanzee–bonobo hybridization. RI from hybrid sterility or inviability was thought unlikely based on the short separation-to-introgression timeline. The forms of RI that typically develop in primates have relatively short timelines (especially for partial implementation); they generally preclude mating or influence hybrid survival and reproduction in certain contexts, and they have the potential to skew introgression directionality. These RI barriers are also consistent with some interpretations of the archaeological and fossil records, especially when behavioral, cognitive, morphological, and genetic differences between the two human species are taken into consideration. Differences potentially influencing patterns of survival and reproduction include interspecies violence, Neandertal xenophobia, provisioning behavior, and ontogenetic, morphological, and behavioral differences affecting matters such as kin and mate recognition, infanticide, and sexual selection. These factors may have skewed the occurrence of interbreeding or the survival and reproduction of hybrids in a way that might at least partially explain the pattern of introgression.

Keywords - Hybridization, Speciation, Introgression.

Introduction RI barriers between them must have been strong (Currat & Excoffier, 2011; Neves & Serva, 2012). Comparison of Neandertal and modern One theoretical model postulating strong human biparentally inherited nuclear DNA has reproductive isolation (RI) between H. nean- been interpreted as demonstrating unidirectional derthalensis and H. sapiens is that of Currat et al. gene flow from Neandertals to some modern (2008), who noted that introgressive genes typi- human populations; this contrasts with data from cally flow from local to invading species in plants uniparentally inherited DNA (mitochondrial and animals; on this view, gene flow simply fol- DNA and Y-chromosome markers), which show lowed the general pattern in introgressing from no evidence of introgression (Gibbons, 2010; resident Neandertals to early modern humans Green et al., 2010; Wall et al., 2009; Yotova et al., expanding out of Africa. Even a small introduc- 2011). Recent theoretical models, over a range tion of local alleles would have the potential to of demographic parameters, have indicated that reach relatively high frequencies because intro- these genetic patterns are predicted if successful duction at the inception of the invasion, no interbreeding events were rare; with evidence of matter how small the total period of interspecies some period of coexistence, this implies that the contact, would have the potential to proliferate

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the alleles widely as a function of demographic locations such as the Near East (i.e., at the bor- change (Currat et al., 2008; Durand et al., 2011; ders of or the overlap between the two ranges). Sankararaman et al., 2012); the H. sapiens popu- Assuming that admixture did occur and that lation was increasing while that of H. neanderthal- the interpretation of unidirectional introgres- ensis was decreasing (Green et al., 2010; Mellars sion is correct (matters still under debate), the & French, 2011). Other factors may also have implication would be that the two human spe- intervened. As Bruner (2013) noted, early mod- cies were reproductively isolated to a significant ern humans and Neandertals may have interbred degree. The implication of strong RI is interest- “to such a negligible degree that evolution and ing and warrants further examination; the ques- selection did not care” (p. 12); further, the phe- tion of what form RI between the two human nomenon of local extinctions could have resulted species might have taken was therefore examined in some interbreeding events leaving traces in the in light of general primate RI tendencies. Future genome while others did not (Green et al., 2010). avenues of research were also suggested for the While the population genetics explanation is archaeological and fossil records and contempo- sufficient to explain the pattern of introgression, rary primatology, consistent with the RI tenden- Currat et al. (2008) acknowledged that their cies of primates, especially baboons (because of model could not explain all cases, since it was their frequent hybridization) and chimpanzees insensitive to complicating factors (e.g., selection and bonobos (because of their genetic similarity functions, preferences and biases, and behaviors) to Neandertals and modern humans). and assumed uniform parameters (e.g., territorial carrying capacities; rates of migration and interbreeding) that might not hold in all cases Previous proposals on RI form or across single cases over time. Several plausible alternatives have also been proposed: Eriksson Hybrid sterility & Manica (2013) interpreted genetic similari- Mason & Short (2011) proposed that the pat- ties as reflecting ancient population structure tern of introgression may demonstrate Haldane’s rather than hybridization, though Sánchez- rule, in which interspecies genetic interactions Quinto et al. (2012) and Yang et al. (2009) have yield differential sex ratios and unisexual sterility in argued that a scenario involving distinct African hybrid offspring (Haldane, 1922). The syndrome subpopulations was unlikely. Gokcumen et al. has been observed in insects, birds, and mammals; (2013) suggested that divergent haplogroups in some species, female hybrids are not produced at mimic the admixture signature, implying that all, are produced infrequently, or are sterile if pro- any introgression would have occurred before the duced, and in others, the syndrome affects male off- two human species diverged. Another a hypoth- spring (Coyne, 1985; Haldane, 1922). Such invia- esis is that of Pinhasi et al. (2011) and Wood et bility or infertility of male hybrids may at least par- al. (2013), who interpreted recent site dating tially explain the apparent lack of Y-chromosome analyses as indicating a minimal contact period; introgression the two human species (Mason & if this is correct, the introgression discussion Short, 2011). Mason & Short (2011) have also will need to incorporate a significantly reduced suggested that the only fertile hybrids were female window of opportunity (especially for Europe), offspring with H. neanderthalensis fathers and H. which would nonetheless be compatible with the sapiens mothers. However, the timeline between H. population genetics explanation. Others have neanderthalensis–H. sapiens separation and intro- noted that the period of coexistence may have gression is relatively short: Their divergence has been extensive, possibly exceeding 10,000 years been estimated to have occurred at a maximum (Currat & Excoffier, 2004; Hublin et al., 2012), of 500,000 years ago and perhaps as recently as with the result that the two human species may 440,000–270,000 years ago (Green et al., 2006, have been constantly in contact, particularly in 2010). The average time for developing hybrid K. A. Overmann & F. L. Coolidge 93

sterility in mammals is less than 2.0 to 4.0 million Neandertal and early modern human remains years (Fitzpatrick, 2004; Wu, 1992), a period of available for comparison; see Bruner, 2013). The time at least double that separating the two human genetic similarity between the two species pairs species. Mason & Short’s (2011) hypothesis would suggests that hybridization would have been therefore require the onset of hybrid sterility to likely for both, given geographic proximity (see have been particularly rapid. Thus, hybrid infertil- the discussion of syngameons, closely related spe- ity appeared unlikely to have been the form of RI cies that hybridize frequently, in Holliday, 2003). isolating the two human species. The timelines and reasons for speciation are parallel between the two species pairs. Other hypotheses Chimpanzees and bonobos speciated less than a Neves & Serva (2012) suggested that H. nean- million years ago, a timeline roughly comparable derthalensis and H. sapiens were reproductively to that separating Neandertals and early modern isolated through cultural or social differences, and humans (Green et al., 2006, 2010; Hey, 2009). Schillachi & Froehlich (2001) proposed that the Both speciation events may have occurred through two human species might have had trouble rec- geographic isolation: Chimpanzees and bonobos ognizing each other as suitable mates. Currat & are thought to have been separated by the Congo Excoffier (2011) also suggested that the two were River, which remains impassible today to their rel- reproductively isolated through lower hybrid fit- atively poor ability to swim (Matsuzawa, 2006). ness; the unidirectionality of the introgression This is analogous to the circumstances believed to suggests that hybrid fitness may have been con- have separated the H. heidelbergensis populations text-dependent. Together, these analyzes suggest ancestral to H. sapiens and H. neanderthalensis, examining archaeological and fossil records, as who were also geographically isolated, perhaps by well as hybridization in other primates, for evi- climate change (e.g., Gipps, 1991). dence of possible behavioral, cognitive, and mor- Chimpanzees and bonobos differ morphologi- phological differences with the potential to have cally and behaviorally, and early modern humans reproductively isolated the two species. and Neandertals might have as well. Morphological differences are subtle, with bonobos being perhaps more paedomorphic (or juvenilized) than The chimpanzee-bonobo model and chimpanzees; paedomorphy represents the com- its extensibility bined effect of heterochronic change in the speed (slowed), onset (late), or duration (shortened) of Hybridization between chimpanzees and ontogenetic growth, with the result that descend- bonobos was considered on the premise that ant adults resemble the ancestral juvenile condi- their case was sufficiently similar to that of H. tion (McKinney, 2000; Schlesinger, 2008; Shea, neanderthalensis and H. sapiens to illuminate 1983a,b). H. sapiens were similarly paedomorphic their potential for and form of RI. Chimpanzees relative to H. neanderthalensis, who may have and bonobos (Pan troglodytes and P. paniscus, matured more quickly and been more robust (Ben- respectively) are the closest genetic relatives of Itzhak et al., 2005; Gunz et al., 2010; Lieberman et H. neanderthalensis and H. sapiens (Green et al., al., 2007; Smith et al., 2010). Behavioral distinc- 2010). The small genetic distance between them tions between chimpanzees and bonobos are more suggests that they could be considered a single overt and include more than three dozen behaviors, species, as has been suggested for H. sapiens and such as cooperation, dispersal patterns, dominance, H. neanderthalensis, who are also known as Homo social structures, provisioning, territoriality, toler- sapiens neanderthalensis (e.g., Curnoe & Thorne, ance, and mating (Hare et al., 2007; Parish & de 2003; Tattersall & Schwartz, 1999; Wegmann & Waal, 2006; Prüfer et al., 2012). H. neanderthalensis Excoffier, 2010; the debate on this has persisted and H. sapiens may also have differed in behaviors for well over a century despite the abundance of such as provisioning, diet, tool production, art, and

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group size (Kuhn & Stiner, 2006; Lalueza-Fox et is prevented, either before or after mating occurs, al., 2011; Richards et al., 2009; Spikins et al., 2010; because species are isolated geographically (i.e., Wynn & Coolidge, 2012). The idea that the two no proximity), temporally (no synchronization of human species differed behaviorally is controversial activity or mating cycles), behaviorally (no recog- (e.g., Villa & Soriano, 2010; Zilhão et al., 2010), nition of mate suitability), mechanically (no fit especially since the complexity of the Levallois between genitalia), or chemically (inability to tol- technique, the use of compound technology, and erate another species’ reproductive environment) the very fact of their long-term survival across wide (Nosil, 2012; Wiens, 2004). In comparison, geographic and climatic ranges argue in favor of in postzygotic RI, hybrids are formed but have Neandertal competency (Roebroeks & Villa, 2011; lower fitness, either in any environment or as a Schlanger, 1996; Stewart, 2005). Nonetheless, function of their ecological circumstance. Lower comparative cranial morphologies and emerging hybrid fitness in any environment would include genetic evidence (discussed below) suggest that the cases in which genomic incompatibility pre- two human species may have differed cognitively, cluded successful embryonic development, as well implying that there would have been behavioral as instances of Haldane’s rule (Haldane, 1922). differences as well. Lower hybrid fitness in certain environments There are several limitations to the chimpan- would include cases in which hybrid survival and zee–bonobo model that constrain its extensibil- reproduction were increased or decreased through ity to the two human species. The first is that factors present in their environmental situation. the morphological, behavioral, and cognitive differences between chimpanzees and bonobos Prezygotic RI appear more subtle than those distinguishing In primates, speciation through prezygotic Neandertals and early modern humans, possi- isolation requires an average of 1.1 million years bly because the former inhabit similar subtropi- (Curnoe et al., 2006). This is slightly longer than cal niches, while the latter inhabited divergent the chimpanzee–bonobo speciation timeline and environments, with Neandertals becoming cold- at least double that of H. neanderthalensis and adapted (Conard, 2011). A second limitation of H. sapiens, suggesting that given the opportunity the model is that the nonhuman pair is distinct– both species pairs might interbreed, as is indeed cognitively, morphologically, and behaviorally– the case with captive chimpanzees and bonobos from the human pair, so that the parallels extend (Curnoe & Thorne, 2003; Vervaecke & Van only so far. A third limitation in the model arises Elsacker, 1992). Notably, RI through prezygotic from the debate on whether H. sapiens and isolation may be the norm for primates (Curnoe H. neanderthalensis differed to any significant et al., 2006); the circumstance that chimpan- degree. That is, interpretations of the archaeo- zees and bonobos have not been separated long logical record as showing no differences between enough to develop it suggests either that H. the two human species argue against RI result- neanderthalensis and H. sapiens were not sepa- ing from morphological, behavioral, or cognitive rated long enough to develop this form of RI, differences, while interpretations of the archaeo- or that their differences (e.g., behavioral, mor- logical record as demonstrating differences argue phological) were significant (and thus might be in favor of RI. detectable in the archaeological record).

Postzygotic RI RI and hybridization In mammals, RI from hybrid inviability requires, on average, between 2.0 and 4.0 mil- RI can be prezygotic or postzygotic (respec- lion years to develop (Fitzpatrick, 2004), at tively, either before or after a zygote is formed). least twice that of prezygotic RI. This average In prezygotic RI, the formation of hybrid zygotes implies that neither species pair would have been K. A. Overmann & F. L. Coolidge 95

reproductively isolated by hybrid inviability, is, though it appears there may have been insuf- since both have shorter timelines. In fact, chim- ficient time for Neandertals and early modern panzees and bonobos produce “apparently nor- humans to develop different forms of RI in a mal” hybrids (Curnoe & Thorne, 2003, p. 211), full and complete manner, there may have been suggesting that Neandertals and early modern sufficient time for them to develop RI barriers humans might have as well. Certainly, other pri- in a partial or incomplete fashion, especially for mate species (particularly baboons) produce fertile prezygotic mechanisms requiring shorter devel- hybrids (e.g., Papio hamadryas and Theropithecus opment times. Partial RI implementation has a gelada; see Dunbar & Dunbar, 1974; Jolly et al., characteristic signature of being skewed since it 1997; Markarjan et al., 1974), though the hybrids precludes only some of the possible outcomes of can also be less successful reproductively, perhaps interbreeding while allowing others. Thus, the as the result of subtle morphological or behavioral specific position on the development continuum differences (Jolly, 2009). (from none to complete) might have influenced RI through hybrid sterility may require less introgression directionality through some une- than 2.0 to 4.0 million years to develop in mam- venness of effect, an assumption more parsimo- mals; assessments are complicated by the fact that nious than assuming uniformity across all pos- hybrid sterility falls on a continuum from partial sible cross-match and circumstantial variations. to complete (Wu, 1992). An example is the case of horses and donkeys, whose speciation occurred Hybridization roughly 3.9 million years ago (based on molecular Hybridization is common among primates data; see Vilà et al., 2001). Female horse–donkey generally and may have occurred between ances- offspring, known as mules and hinnys, are usually– tral chimpanzees and the hominin lineage fol- but not invariably–sterile (Rong et al., 1988; Rong lowing speciation from the last common ances- et al., 1985). This suggests that the development tor (Aguiar et al., 2008; Patterson et al., 2006; of hybrid sterility in horses and donkeys is nearly Zinner et al., 2011). This suggests that the will- complete, in affecting all male and most female ingness to breed across species might character- hybrids, but nonetheless falls short of being total. ize both descendent lineages, a supposition con- This state was reached in four times the amount of firmed by the fact that chimpanzees and bonobos time separating bonobos from chimpanzees and will interbreed in captivity (Curnoe & Thorne, eight (or more) times that separating Neandertals 2003; Vervaecke & Van Elsacker, 1992). The and early modern humans. Thus, even if primates morphology of primate hybrids is highly vari- developed hybrid sterility at an accelerated rate able but generally intermediate between that of relative to mammals (which they are not known the two parent species; morphs can range from to do), there may still have been insufficient time being indistinguishable from either parent spe- for it to have developed in H. neanderthalensis–H. cies (cryptic), in between the two (intermediate), sapiens hybrids. The idea that the time was insuffi- or outside the range of variation of either (unu- cient is further reinforced by the circumstance that sual) (Ackerman, 2010; Zinner et al., 2011). In chimpanzee–bonobo hybrids are probably fertile, addition to morphological intermediacy, behav- something that is difficult to confirm because of ioral intermediacy has been observed in mam- legal restrictions on their breeding (Vervaecke, mal hybrids (e.g., Weber et al., 2013). Notably, personal communication). chimpanzee–bonobo hybrids are characterized by both morphological and behavioral interme- RI variation diacy (Vervaecke, personal communication). In Since RI through hybrid sterility exists on a general, some hybrids are more vigorous, some continuum (Wu, 1992), other forms of RI may less, than the two parent species (Ackerman, as well, possibly accounting for some of the 2010); chimpanzee–bonobo hybrids have been insufficiencies in the speciation timeline. That described as having normal vitality, though this

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observation relates to circumstances of captiv- distance between the two human species was ity (Curnoe & Thorne, 2003). By extension, H. smaller than that between some modern human neanderthalensis–H. sapiens hybrids might have populations (Curnoe & Thorne, 2003; Neves & had morphological and behavioral characteristics Serva, 2012). Behavioral, cognitive, and morpho- that were generally intermediate between their logical differences do not prevent chimpanzees two parent species, and while their vitality might and bonobos from interbreeding, at least under have been normal, it could also have been a fac- the choice-restricted circumstances of captivity, or tor in their ability to respond to specific environ- from producing hybrids of apparent normality, as mental conditions. assessed against the artificial conditions of captivity (Curnoe & Thorne, 2003; Vervaecke & Van Forms of RI observed in primates Elsacker, 1992). In addition, the four chimpanzee Prezygotic RI (the primate norm; see Curnoe subspecies – P. t. schweinfurthii, P. t. troglodytes, P. t. et al., 2006) and lower hybrid fitness (postzygotic vellurosus, and P. t. verus – are similarly isolated by RI) have been observed in primate hybridization geography and differentiated by their behavior and (Aguiar et al., 2008). Asymmetric gene flow from morphology; however, they are known to inter- postzygotic RI has also been observed in pri- breed both in the wild and in captivity and have mates (e.g., Macaca mulatta and M. fascicularis; been said to do so in all combinations (Becquet & see Stevison & Kohn, 2009), with behavior (e.g., Przeworski, 2007; Fischer et al., 2004; Gagneux philopatry; dispersal) and social group structure et al., 2001; Hey, 2010; Matsuzawa, 2006; Won influencing gene flow and population structure & Hey, 2010). These circumstances suggest either (Tung et al., 2010). These RI barriers and influ- that the differences between Neandertals and early ences, coupled with a timeline that may preclude modern humans were more profound than those the development of RI between H. neanderthal- distinguishing chimpanzees and bonobos (pre- ensis and H. sapiens in any form but especially in cluding mating), or that interbreeding between the forms of hybrid inviability and sterility, sug- the two human species was common but factors gests that if the two human species were reproduc- such as higher hybrid morality influenced hybrid tively isolated, the form it might have taken would survival and reproduction and hence the direc- have followed these primate tendencies. That is, if tionality of the introgression–or both, since the H. neanderthalensis and H. sapiens were reproduc- two are not mutually exclusive. tively isolated, it may have been through behaviors Apparently no barrier to interbreeding, chim- that prevented the occurrence of mating, through panzee–bonobo behavioral differences none- lower hybrid fitness if mating did occur, or both. theless imply cognitive differences between the two nonhuman species; for example, the greater ‘patience’ of bonobos relative to chimpanzees Interbreeding between implies a difference in inhibition, an executive H. neanderthalensis and H. sapiens function (Rosati et al., 2007). These cognitive differences are consistent with the endocranial differ- The question posed by the chimpanzee– ences between the two species, which result from bonobo model, in which interbreeding between the divergent ontogenetic trajectories followed by species is common (at least in captivity) and each (Durrleman et al., 2012; Mitteroecker et al., productive (in terms of hybrid vitality and possi- 2005). The assumption that cognition may have bly hybrid fertility as well), is why interbreeding similarly distinguished H. neanderthalensis and between H. neanderthalensis and H. sapiens would H. sapiens may not be unwarranted, given that have been rare once the populations reencountered morphometric differences in their fossil endocasts one another (Currat & Excoffier, 2011; Currat et imply differences in cognitive domains such as al., 2008; Neves & Serva, 2012). The assump- language, spatiality, and creativity (e.g., Bruner, tion of strong RI is curious given that the genetic 2004, 2010; Bruner et al., 2003; Coolidge & K. A. Overmann & F. L. Coolidge 97

Wynn, 2013; Gunz et al., 2010; Lieberman et al., to higher-level capabilities for symbolism 2002; Pearce et al., 2013). The idea that there were (Coolidge & Overmann, 2012). differences in cognitive functioning is consistent The H. sapiens cerebellum may also have dif- with archaeological interpretations of behavioral fered. Weaver (2005) found mean cerebellum differences (e.g., Coolidge & Wynn, 2001, 2004; volume to be absolutely and relatively higher in Henshilwood & Marean, 2003; Mellars, 2004; modern H. sapiens than in H. neanderthalensis, Wynn & Coolidge, 2004, 2012). and further, a derived cerebellar quotient (cerebellum/overall brain volume) was also larger in H. Anatomic evidence with cognitive implications sapiens than in H. neanderthalensis (however, a Morphometric comparison of H. neander- caveat is in order: Weaver’s study involved small thalensis and H. sapiens endocasts reveals differ- samples, limited metrics, and straightforward sta- ences in asymmetry, the relative size and shape tistical analyses). Every major lobe of the cortex of the major lobes, and the cerebellum. Greater projects through the pons to the cerebellum, and frontal–temporal encephalization and differential the cerebellum through the thalamus reciprocally asymmetry patterns in H. sapiens suggest a language connects to at least 14 neocortical sites. While advantage for that species, enabling more effective early theories of cerebellar function proposed that communication between individuals (social coop- motor learning and fine motor control were key eration) and across time (cultural learning) (Gunz attributes, recent research has clearly established et al., 2010; Lieberman et al., 2002;). Frontal lobe that the cerebellum has an important role in non- volume appears relatively equal between the two motor cognitive functions as well, particularly species (Bruner & Holloway, 2010), so differences with its interconnections to the prefrontal corti- in executive functioning cannot be determined by ces and to the parietal lobes. Balsters et al. (2013) morphometric analysis and endocast comparison demonstrated that cerebellar lobules (Crus I & II) alone. However, differential executive functioning have prefrontal-projecting connections activated may reflect differential neural reorganization sub- when processing first- and second-order cognitive sequent to encephalization (both human species) (non-motor) instructions. Weaver (2005) further or globularization (H. sapiens only) (Coolidge & argued that cerebellar development in H. sapiens Wynn, 2001). may have provided greater computational effi- Bruner and colleagues (Bruner, 2004, 2010; ciency and adaptive ability. Koziol et al. (2010) Bruner et al., 2003) have suggested that parietal attributed greater speed of adaptation and behav- change may be the characteristic that truly distin- ioral mastery and refinement to cerebellar devel- guishes the two human species: The parietal region opment, and Vandervert (2009, 2011) attributed of early modern humans has an expansion (prob- creativity, giftedness, and the neural basis for child ably in the intraparietal sulcus, medial region, or prodigies to the efficiency and nature of the ce- upper cortex) not found in Neandertals. Parietal rebrum–cerebellar loops. The smaller Neandertal expansion has been associated with globulariza- cerebellum may therefore imply a difference in tion, neural reorganization, and enhanced parietal creativity, which would be consistent with archae- functioning, including multimodal processing, ological interpretations suggesting behavioral dif- visuospatial and sensory integration, planning ferences between the two human species (e.g., and manipulation of motor sequences, control of Coolidge & Wynn, 2001, 2004, 2005; Wynn & fingers, spatial analysis, and the creation of ‘inner Coolidge, 2002, 2004, 2012). space’ representations of external space (Bruner, Pearce et al. (2013) also noted that the larger 2004, 2010; Bruner et al., 2003). Thus, parietal portion of the Neandertal brain dedicated to change may have contributed to the adaptive suc- vision implied both a visual difference at higher cess of H. sapiens through improved multimodal latitudes and a corresponding reduction in the size integration, visuospatial integration, and social of other brain regions; the relative resizing of non- functioning (Holloway, 1996) or by contributing occipital regions of the Neandertal brain implies

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concomitant differences in their cognitive func- the two human species, differences with the poten- tionality because of the relationship between brain tial to contribute to RI. Behaviors and behavioral region size and functionality (Striedter, 2005). differences that possibly acted to reduce or preclude interbreeding are suggested by evidence of inter- Genetic evidence with cognitive implications group violence, Neandertal xenophobia, and differ- Emerging genetic evidence suggests there ential provisioning and dispersal. As shown in Table were at least subtle differences in the cognitive 1, intergroup violence and Neandertal xenophobia abilities of H. neanderthalensis and H. sapiens: might have reduced the likelihood of interbreeding Paixão-Côrtes et al. (2013) found nine non-syn- across the board, and differences in provisioning onymous substitutions (i.e., substitutions result- behavior might have increased the likelihood of ing in biological change and therefore subject interbreeding between H. neanderthalensis males to natural selection) in genes implicated in vari- and H. sapiens females. The effect of dispersal pat- ous forms of learning and memory; these imply tern differences was uncertain. that the two human species may have differed in these cognitive domains, as has been sug- Intergroup violence gested by Wynn & Coolidge (2004). The nine As “many kinds of primates are intolerant of non-synonymous substitutions were 10% of 93 strangers,” a factor in the formation of breeding alleles examined in the study; Neandertal data groups (Erwin, 1986, p. 297), interspecies violence for another 27% were missing, admitting the related to territoriality might have discouraged possibility that additional genetic changes with contact between groups, thereby reducing mating cognitive implications may be found. While the opportunities. While baboons do not appear to be 10% difference presently identified would not particularly territorial (Cowlishaw, 1995; Howell decrease, were the missing data to vary at the & Bourlière, 2008), wild chimpanzees have been same rate, the difference would show a minor known to engage in cooperative defense and even increase (12%) but could increase to as much patrol their territories, influencing female repro- as 37% in the unlikely case that all 25 cases of ductive behavior (Mitani & Watts, 2005; Mitani missing data differed. In view of studies show- et al., 2010; Williams et al., 2004; Williams et al., ing that a single gene can significantly alter the 2004; Wilson et al., 2001). Violent contact between brain (e.g., Bakircioglu et al., 2011), the study the two human species is suggested by Shanidar-3, by Paixão-Côrtes et al. (2013) suggested that the the Neandertal skeleton from Shanidar, Iraq whose genetic differences identified (plus any additional ninth rib is lesioned in a way that would be con- instances identified once the missing Neandertal sistent with the projectile weapons of early mod- data have been established) should be investi- ern humans (Churchill et al., 2009; Santamaria et gated for their impact on cognition, learning, al., 2010); actuarial support for weapons produc- and memory, especially short-term and visual ing similar wounds cannot, however, be taken as memory, cognitive abilities potentially affected proof that Neandertals and early modern humans by the contribution and interaction of seven or were in contact, let alone in conflict. However, more non-synonymous substitutions. some interpretations of the archaeological evidence have suggested that whatever contact limitations were in place at the beginning of the coexistence Behaviors in the archaeological period may have improved toward its end, based on record and other primates Neandertal techno-cultural changes that imply prolonged, amiable contact with early modern humans Anatomic and genetic evidence of potential (Green et al., 2006; Hublin et al., 1996; but also see cognitive differences between Neandertals and early Higham et al., 2010, who highlight the challenges modern humans are consistent with archaeological of establishing clear associations between artifacts interpretations of behavioral differences between and their makers). K. A. Overmann & F. L. Coolidge 99

Neandertal xenophobia Tab. 1 - Influence of differential behavior and An aspect of group-level intolerance of stran- morphology. gers is that of possible Neandertal reluctance to approach strangers (xenophobia), which might Potential F: Hn; F: Hs; have reduced the likelihood of their approaching Influence on RI M:Hs M:Hn human individuals for any reason, including mating. The characterization of Neandertals as shy is Behavior based on archaeological evidence of their living Intergroup Violence Reduce Reduce in small groups and generally lacking exotic raw Neandertal Xenophobia Reduce Reduce materials at their sites, factors interpreted by some scholars as suggesting that Neandertals may have Provisioning Increase Reduce had difficulty managing numerous face-to-face Dispersal Uncertain Uncertain contacts and relatively restricted territorial mobility that imply possible cognitive constraints on sociality and spatiality, respectively (Fernández- Morphology Laso et al., 2011; Gamble, 2011; Gamble et al., Ontogenetic Differences Increase Uncertain 2011; García-Antón et al., 2011; Lalueza-Fox et al., 2011; Wynn & Coolidge, 2004, 2012). Sexual Selection Increase Reduce However, this possible influence on interbreeding must be tempered by the insight that Neandertals Note - Key: F = Father; M = Mother; Hn = H. neanderthalensis; may not have been as territorially restricted as Hs = H. sapiens. The overall pattern suggested an increased once thought; for example, recent evidence of likelihood of interbreeding between H. neanderthalensis males diet and raw material exploitation suggests that and H. sapiens females and a reduced likelihood of interbreed- they may have exploited larger territories and ing between H. neanderthalensis females and H. sapiens males. had less restricted diets than previously believed (Richards et al., 2008, 2009; Spinapolice, 2012). interference and protection would have been less likely, as remains the case in modern situations (e.g., Koshen, 2007). Conspecific interference is Provisioning behaviors certainly a behavior observed in wild chimpan- Communal hunting by Neandertals, with zees (e.g., Williams et al., 2004). However, the gathering plus gendered division of labor by early inclusion of gathering as a provisioning strategy modern humans (Kuhn & Stiner, 2006; Richards by Neandertals (Hardy et al., 2012) and the phe- et al., 2009), imply differential opportunities for nomenon of H. sapiens female hunting in mod- mating and conspecific interference, factors that ern hunter–gatherer societies (Kuhn & Stiner, could have reduced or prevented interbreeding. 2006) suggest that there may have been a signifi- That is, the inclusion of both Neandertal males cant amount of commonality in the provisioning and females in hunting groups suggests that both behaviors of both human species, with the result sexes were less likely to be unaccompanied and that the contribution of behavioral differences in thus less likely to be in situations in which mat- provisioning to RI requires further examination. ing could occur, whether opportunistic or coer- cive (Buss, 2007). By comparison, human males Dispersal patterns engaged in hunting may have been more likely Differences in age- or sex- based dispersal unaccompanied or have had group dominance patterns may have affected the occurrence of advantages that would facilitate mating, while interbreeding. For age, dispersal-pattern differ- human females engaged in gathering would ences have been noted in baboon hybrids (P. anu- more likely have been unaccompanied or in bis and P. cynocephalus; see Alberts & Altmann, female-only situations in which conspecific male 2001), suggesting that H. neanderthalensis–H.

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sapiens hybrids may have dispersed at a differ- Mate recognition and ontogenetic differences ent age than non-hybrids. Regarding sex-based Neandertals may have matured faster (and differences, Neandertals may have been male thus earlier), based on evidence showing that philopatric, a primate social system in which they had shorter periods of dental development males remain in their natal range while females than was typical for early modern humans (Smith reaching sexual maturity emigrate to new groups et al., 2010; but also see Guatelli-Steinberg et al., (Lalueza-Fox et al., 2011). Genetic evidence 2005, who note that Neandertal dental growth supporting this hypothesis derives from 12 rates fall within the human range). Cranial Neandertal remains at El Sidrón, Asturias, Spain, development may have differed as well, with H. which show three different maternal lineages for sapiens developing a more globular brain shape all 12 individuals but the same mitochondrial postnatally that implies a longer period of neural DNA for the three adult males (but also see reorganization than would have been the case for Vigilant & Langergraber, 2011, who argue that H. neanderthalensis, who lacked postnatal glob- this evidence is inconclusive at best). In com- ularization (Gunz et al., 2010). This suggested parison, 70% of all modern human societies are that brain development (and thus immaturity) patrilocal (a related and fairly synonymous term would have been prolonged in H. sapiens relative for a social system in which married females to H. neanderthalensis (however, also see Ponce de reside with their husband’s family; the terms may León et al., 2008, who suggest that brain growth be differentiated along lines of humans [patri- rates were similar in both human species). These local] and nonhumans [male philopatry]; see potential differences in maturity, if substanti- Chapais, 2008). The rate for H. sapiens has been ated by future studies, might have been a fac- estimated by some researchers as greater than tor in dispersal patterns and mate recognition, that of modern chimpanzees, which are strongly enhanced for the earlier-maturing Neandertals biased toward male philopatry and female dis- and degraded for later-maturing early modern persal (Hashimoto et al., 2008; Langergraber et humans. Such is the case for hybrid baboons, al., 2007; Matsuzawa, 2006). However, Parish with hybrids of both sexes maturing and dispers- & de Waal (2006) have reported lower estimates ing earlier, resulting in a selective advantage for of patrilocality for humans and have suggested hybrid males (advantages for female hybrids are that there is no typical pattern of female dispersal offset by other social and environmental factors; for hunter–gatherers. Differences in the degree see Alberts & Altmann, 2001; Charpentier et al., of philopatry between the two human species 2008; Tung et al., 2008). might therefore have had the potential to skew the pattern of interbreeding. Mate recognition and sexual selection As previously noted, H. sapiens were pae- Morphology in the fossil record and domorphic relative to H. neanderthalensis, who other primates were characterized by greater muscle mass and bone strength (Ben-Itzhak et al., 2005; Gunz et The morphological differences between al., 2010; Lieberman et al., 2007; Smith et al., the two human species seen in fossils may have 2010). These physiological differences might influenced mate recognition through factors of have influenced mate recognition, especially in ontogenetic development and sexual selection; female choice: H. neanderthalensis females might this is distinct from the idea of trying to recognize have interpreted paedomorphic H. sapiens males hybrid morphology in fossils (Holliday, 2003). as having unsuitable youthfulness or lower fitness, As shown in Table 1, ontogenetic differences thereby reducing their recognition as suitable and sexual selection may have provided possible mates. It is also possible that H. sapiens females advantages for H. neanderthalensis males. might have interpreted the earlier maturing, K. A. Overmann & F. L. Coolidge 101

more robust H. neanderthalensis male form as Tab. 2 - Influence on hybrid fitness. indicating suitability for mating and higher fitness. A similar pattern might be predicted for Potential Hybrids Hybrids among Influence among H. neanderthalensis chimpanzees and bonobos (i.e., that there would on RI H. sapiens be female selection differences depending on the particular combination of paedomorphic vs. Survival Increase Reduce robust species); however, the literature on chim- (Morphology) panzee–bonobo hybridization does not address Infanticide Reduce Reduce whether this has been observed, and in any case the influence of captivity on opportunity and Survival Reduce Reduce choice would have to be considered as well. The (Behavior) effect has been observed in macaques, however, Kin Reduce Reduce with introgression “biased strongly” toward M. Recognition mulatta males (the larger species) and M. fascicularis females (the smaller species), either because Note - The overall pattern suggested that hybrids might have the females prefer the larger males or because the had a slightly better chance of surviving among H. sapiens larger males can more easily coerce sex (Stevison than among H. neanderthalensis. & Kohn, 2009, p. 2470), biases that might also have also characterized Neandertal males and and megaherbivores (e.g., mammoth, wooly early modern human females (see Mason & rhinoceros); the combination caused severe, Short, 2011, who note the strength differential). often fatal injuries (Berger & Trinkaus, 1995; The tendency is also found in baboon hybrids: Bocherens, 2011; Gaudzinski-Windheuser & P. hamadryas and P. Anubis hybrid males have a Roebroeks, 2011). The trauma patterns are con- phenotype that is apparently more attractive to sistent with other fossil evidence of young–old females (Nystrom, 1992). differentials suggestive of early mortality for Neandertal adults and a generally high rate of mortality for Neandertal infants (Pettitt, 2000; Hybrid fitness mediated by context Richter, 2001; Trinkaus, 1995, 2011). Given the intermediate morphology of chimpanzee–bonobo Morphological and behavioral intermediacy hybrids, it is likely that H. neanderthalensis–H. for H. neanderthalensis–H. sapiens hybrids may sapiens hybrids would also have taken an inter- have influenced the directionality of introgres- mediate form as well (consistent with the vari- sion by reducing their fitness or by reducing ability noted by Ackerman, 2010). In general, mate or kin recognition. As shown in Table 2, hybrids might have been less robust in terms of intermediacy in hybrid morphology possibly muscle mass and bone strength than was typical provided an advantage to hybrids among early for Neandertals but stronger and more robust modern humans but a disadvantage for hybrids than usual for early modern humans (Ben-Itzhak among the Neandertals. In addition, uncertain et al., 2005), a potential disadvantage for hybrids paternity, hybrid behavioral intermediacy, or among the Neandertals but a potential advantage weakened kin recognition might have reduced among early modern humans, possibly influenc- hybrid survival in either situation. ing the direction of introgression.

Lower survival outcomes from intermediate hybrid Infanticide morphology Intermediate and unusual (but possibly not Fossil trauma patterns suggest that the cryptic) hybrids on both sides might have been Neandertal led an arduous, dangerous lifestyle subjected to infanticide, a consequence of the that included close-in hunting of large animals greater likelihood of their being recognized as

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having uncertain paternity (a significant cause of in executive functioning, including inhibition infanticide across primate species; see Hiraiwa- (Coolidge & Wynn, 2001, 2004, 2005; Wynn Hasegawa, 1988) or to reduce the competition & Coolidge, 2002, 2004, 2012), a possible factor for resources (Hrdy, 1979). The latter may have in hybrid survival. However, while cognitive dif- been particularly true for non-cryptic hybrids ferences can be inferred from the morphological among the Neandertals, given the range of comparison of fossils, similar inferences of behav- potential factors contributing to the species’ ioral differences from archaeological remains are demographic decline and eventual extinction. open to interpretation. Nonetheless, the greater Infanticide has been practiced by many human rate of traumatic injury in Neandertals might be groups, including contemporary ones, and has consistent with higher levels of risk-taking, sug- been observed in modern chimpanzees, where it gesting that hybrid behavioral variability could has been interpreted as the result of male aggres- have been a survival factor. sion, pathological female cannibalism for the sake of nutritional advantage, or the selection of Reduced mate and kin recognition particularly vulnerable targets during inter-group Another potential outcome of hybrid inter- violence (Sherrow & Amsler, 2007; Townsend mediacy might have been reduced mate and kin et al., 2007). Male aggression against infants recognition, which has been observed in primate has also been observed in baboons (Cowlishaw, hybrids (e.g., Bradley & Mundy, 2008; Jolly, 1995). The greater likelihood of being subject to 2009). For example, P. hamadryas interbreeds infanticide might have reduced hybrid survival in with M. mulatta, but the resultant hybrids are both groups, especially among the Neandertals. less reproductively successful, either because they are not recognized as suitable mates or they are infertile (Jolly, 2001, 2009; Markarjan et al., Lower survival outcomes from intermediate hybrid 1997). Across primate species, mechanisms used behavior for mate and kin recognition include pheno- Hybrid males, assuming they survived past typic matching and behavioral cues (Silk, 2005; infancy, might have been more aggressive than Strier, 2004), mechanisms potentially weakened the norm (hybrid behavioral intermediacy) or by hybrid morphological and behavioral vari- less able to inhibit aggressive impulses (hybrid ability and possibly exacerbated by Neandertal cognitive intermediacy), creating situations of xenophobia. The likelihood of survival might early mortality through risky behavior, or exile or have been decreased further by the demands of attack from an inability of the group to tolerate the Neandertal lifestyle, especially given the lack abnormal levels of behaviors such as aggression. of older individuals available to assist with provi- Such behaviors and consequences are known sioning and infant care (Trinkaus, 1995, 2011); among modern chimpanzees and humans (e.g., among H. sapiens, these conditions were perhaps Nishida, 2004; Nishida et al., 1995; Townsend et not as severe, with the result that the likelihood al., 2007; Wrangham & Peterson, 1996), imply- of survival may have been marginally better. ing that they might also have characterized the Neandertals as well. Behavioral comparisons of chimpanzees and bonobos suggests that bonobos, Conclusions the more paedomorphic species, are less aggressive and display greater inhibition (an executive func- The pattern of introgression detected in com- tion) than chimpanzees (Hare et al., 2007; Parish parison of the H. neanderthalensis and H. sapiens & de Waal, 2006; Prüfer et al., 2012; Rosati et al., genomes (Green et al., 2010) may not have been 2007). A comparison of the cognitive capabilities the result of hybrid sterility (Mason & Short, of Neandertals and early modern humans suggests 2011) because of the insufficient amount of time that the latter may have had similar advantages between the separation and reunion of the two K. A. Overmann & F. L. Coolidge 103

human species, nor of hybrid inviability, which acceptance within natal groups that might extend requires at least as much time (if not more) to to non-natal groups as well. A second limitation instantiate. However, introgression directional- of the review was that the effect of hybrid gender ity could have been influenced by forms of RI on survival and reproduction was not considered that are typical for primates–specifically, prezy- in detail, something future studies might address. gotic (premating) isolation and postzygotic survival and reproduction differentials–given two assumptions: first, that behavioral, mor- Acknowledgements phological, and cognitive differences (which are consistent with emerging genetic evidence) We are grateful for the contributions of Jeremy Bono, were sufficient to influence matters such as mate Professor of Biology at the University of Colorado, recognition and sexual selection; second, that Colorado Springs, who reviewed early drafts of this hybrid intermediacy was sufficient to influence article, and Dr. Emiliano Bruner and three anony- survival and reproduction outcomes. While these mous referees, whose close and critical review of the RI mechanisms may have skewed the pattern of manuscript led to significant improvements in it. interbreeding and hybrid survival and reproduction, all of them require a more in-depth examination of the archaeological and fossil records, as References well as comparisons with modern primate species that hybridize (especially baboons, chimpanzees, Ackerman R.R. 2010. Phenotypic traits of pri- and bonobos). If interbreeding between the two mate hybrids: recognizing admixture in the fos- human species was more likely to have involved sil record. Evol. Anthropol., 19: 258–270. H. neanderthalensis males and H. sapiens females, Aguiar L.M., Pie M.R. & Passos F.C. 2008. Wild and survival and reproduction outcomes were mixed groups of howler species (Alouatta caraya better for hybrids among early modern humans and Alouatta clamitans) and new evidence for but lower for hybrids among the Neandertals, their hybridization. Primates, 49: 149–152. these factors may be apparent from the archaeo- Alberts S.C. & Altmann J. 2001. Immigration logical and fossil records, as well as tendencies and hybridization patterns of yellow and anubis observed in contemporary primate species. baboons in and around Amboseli, Kenya. Am. A limitation of the present review was that it J. Primatol., 53: 139–154. assumed that hybrids would remain with their Balsters J.H., Whelan C.D., Robertson I.H. & natal groups to interbreed with the species rais- Ramnani N. 2013. Cerebellum and cognition: ing them if they survived to sexual maturity and evidence for the encoding of higher order rules. were recognized as suitable mates. It is of course Cereb. Cortex, 23: 1433–1443. possible that hybrids might not have remained Bakircioglu M., Carvalho O.P., Khurshid M., Cox with their natal groups, instead moving between J.J., Tuysuz B., Barak T., Yilmaz S., Caglayan groups of different species, perhaps with greater O., Dincer A., Nicholas A.K., Quarrell O., ease and acceptance than might have been the Springell K., Karbani G., Malik S., Gannon C., case for non-hybrids. However, this possibility Sheridan E., Crosier M., Lisgo S.N., Lindsay reflects a level of granularity seldom reached in S., Bilguvar K., Gergely F., Gunel M. & Woods fossil analysis, since hybrid phenotypes are diffi- C.G. 2011. The essential role of centrosomal cult to disambiguate from inter-individual varia- NDE1 in human cerebral cortex neurogenesis. tion (Ackerman, 2010). Observational data from Am. J. Hum. Genet., 88: 1–13. nonhuman primates might determine whether Becquet C. & Przeworski M. 2007. A new ap- hybrid acceptance varies across primate groups proach to estimate parameters of speciation generally, though the reduced reproductive suc- models with application to apes. Genome Res., cess of hybrids (Jolly, 2009) suggests a decreased 17: 1505–1519.

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