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Journal of Anthropological 35 (2014) 32–50

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Journal of Anthropological Archaeology

journal homepage: www.elsevier.com/locate/jaa

The place of the in hominin phylogeny ⇑ Suzanna White, John A.J. Gowlett, Matt Grove

School of Archaeology, Classics and Egyptology, University of Liverpool, William Hartley Building, Brownlow Street, Liverpool L69 3GS, UK article info abstract

Article history: Debate over the taxonomic status of the Neanderthals has been incessant since the initial discovery of the Received 8 May 2013 type specimens, with some arguing they should be included within our species (i.e. sapiens nean- Revision received 21 March 2014 derthalensis) and others believing them to be different enough to constitute their own species (Homo Available online 13 May 2014 neanderthalensis). This synthesis addresses the process of as well as incorporating information on the differences between species and subspecies, and the criteria used for discriminating between the Keywords: two. It also analyses the evidence for –AMH hybrids, and their relevance to the species Neanderthals debate, before discussing morphological and genetic evidence relevant to the Neanderthal taxonomic debate. The main conclusion is that Neanderthals fulfil all major requirements for species status. The Species status extent of interbreeding between the two populations is still highly debated, and is irrelevant to the issue at hand, as the Biological Species Concept allows for an expected amount of interbreeding between species. Ó 2014 Elsevier Inc. All rights reserved.

Introduction AMH are innately different to other organisms. This article aims to draw from taxonomic biology, identifying the methods of distin- Neanderthals were given the Linnaean name of Homo neander- guishing species and subspecies before assessing the relevant mor- thalensis after King’s (1864) description of the original type-speci- phological and genetic evidence, as well as the supposed direct mens, which he felt were so different from modern Homo sapiens evidence of interbreeding between these two populations in the that they may even represent a new . King’s (1864)view con- form of hybrids. trasts with Huxley’s (1863) classification of Neanderthals as a sub- species of (Homo sapiens neanderthalensis), owing to the The species ‘problem’ latter’s belief that they could be included in Linnaeus’ (1802) H. sapiens despite their primitive (Tattersall, 2007). The debate The ‘species problem’ is largely a result of the philosophy and continues into modern research, with some believing Neanderthals history of the field of taxonomy (Ghiselin, 1974). The main issues are sufficiently differentiated to constitute a separate species (e.g. can be assigned to three categories: definition and concepts of Tattersall, 1986; Holliday, 2006), and others disagreeing (e.g. what constitutes a ‘species’; the speciation process; and debates Dobzhansky, 1944; Currat and Excoffier, 2004). A recent preference concerning criteria for species identification (Simpson, 1961; de for the species classification has arisen (de Vos, 2009), although a Queiroz, 2005). While species are fundamental to the study of evo- group of recent papers using studies of the Neanderthal genome lution (Tattersall, 1986), they are considered by some to be arbi- (Green et al., 2010; Mendez et al., 2012; Wall et al., 2013) strongly trary (Dobzhansky, 1935; Foley, 1991), and to lack a single indicating interbreeding between Anatomically Modern reality over a geographic and temporal range (Simpson, 1951; (henceforth AMH) and Neanderthals, has re-awakened the debate. Foley, 1991; Mallet, 2007). There is a very real need to return to the rules and methods of traditional taxonomy to further our understanding of what species Definition of ‘species’ are and how to identify them. The use of such classification sys- tems is essential for valid conclusions, as they are based on univer- The first problem lies in an inconsistency in the use and meaning sal patterns found in all species, and thus have to be applicable, of the term ‘species’. Different definitions include: a rank in a Lin- despite inherent anthropocentrism and a subsequent belief that naean hierarchy using individual attributes to encompass all organ- isms at the species level (Quicke, 1993; Mayr, 1996), the end ⇑ Corresponding author. product of speciation (Nixon and Wheeler, 1990; Shaw, 1998), or E-mail address: [email protected] (M. Grove). the concept of what it is to be a species and what this category http://dx.doi.org/10.1016/j.jaa.2014.04.004 0278-4165/Ó 2014 Elsevier Inc. All rights reserved. S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 33 represents (Kimbel and Rak, 1993; de Queiroz, 1998). Issues arise 23 (Quintyn, 2009). The eight main concepts with relevance to this over the inherent tautology of definitions, with species frequently matter are summarised in Appendix A. being defined as ‘whatever a competent taxonomist says is a spe- The definitions of species provided by the Phylogenetic and cies’ (Quicke, 1993). Evolutionary Species Concepts are readily applicable to the Nean- The nature and definition of species is intimately linked to the derthal species debate, and would support species status in the process of speciation, as species are dynamic parts of this overall sense that there is a consistent use of morphology to identify Nean- process (Harrison, 1998) and can therefore only be an abstract cat- derthal specimens and that this population eventually arrived at egory (Dobzhansky, 1935). Speciation in is a gradual extinction. The Recognition Concept (Paterson, 1981) identifies process not an instantaneous event (Simpson, 1951; Mayr and species through species-specific mating recognition systems Ashlock, 1991; de Queiroz, 1998), which means we should expect (SMRS), which have been tentatively inferred in fossil hominins. to find organisms representing the entire panoply of stages, not For instance, as Neanderthals and AMH are clearly different in just the end product (Mayr, 1964, 1996; Mayr and Ashlock, appearance to palaeoanthropologists, they must at least represent 1991). Five such stages have been proposed for gradualistic speci- different subspecies (Tattersall, 1992). However this concept has ation: local populations, subspecies, semi-species, sibling species, been said to overestimate (Tattersall, 1992) or underestimate and morphologically different species (Masters, 1993), yet distin- (Kimbel, 1991) the number of species, as skeletons do guishing between these stages is more difficult. not have obvious morphological features that can be linked to SMRS (Kimbel, 1991), and its tautological nature has been revealed upon application to extant (Jolly, 1993). Species concepts Most debate over species classification uses the Biological Spe- cies Concept proposed by Mayr (1964) and Dobzhansky (1935), Most debate is over the true ‘concept’ of species (Hey, 2006), as which defines species as reproductively isolated populations. frameworks for study and identification of species are dependent According to the criterion of complete reproductive isolation, on the researcher’s species concept (Quintyn, 2009). All concepts Neanderthals and AMH would have to be classified as the same are arbitrary to some extent (Reydon, 2004), with different con- species if interbreeding did occur. Yet this strict criterion was cepts producing different numbers of taxa (Foley, 1991; objected to by both Darwin and Wallace. Wallace took his objec- Balakrishnan, 2005). Some have argued that the ‘Species Concept’ tion further by highlighting the circular reasoning of defining and problem is itself a fallacy, as all researchers seem to agree on one delimiting a taxon by the same criteria (Mallet, 1995). The require- concept in the linguistic sense at least, with species being the tip ment of complete reproductive isolation is a common misconcep- of an evolutionary lineage (Hey, 2006). Fig. 1 gives an indication tion: Mayr himself acknowledged that occasional hybridisation of the complex development of this area of the philosophy of tax- occurs between sympatric species (Mayr, 1964, 1996), as isolation onomy, with the number of current species concepts being at least mechanisms do not prevent all interbreeding, with their main role

Fig. 1. ‘Phylogeny’ of species concepts (Quintyn, 2009: 310). 34 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 being protection of a harmonious gene pool (Mayr, 1996). As shall that it can be applied to most cases, but involves a subjective deci- be shown, interbreeding freely occurs between different taxo- sion over which traits to use (Boggs, 2001). nomic levels without compromising species status. Most accept As can be seen, the primary criteria (for fossils at least) are mor- the main principles of this concept and use it to provide practical phological, with the assumption being that morphology approxi- guidelines (Tattersall, 1992), overcoming the main issues by mod- mates genetic differences (Simpson, 1943). This ‘morphospecies’ ifying and supplementing this concept with other, more appropri- concept is the main method used in palaeontological taxonomy ate concepts (Simpson, 1951). (Holliday, 2003) due to its practicality. However the evolutionary meaning of such groups is speculative at best (Holliday, 2003; Species criteria and methods of delimitation Ahern, 2006). In addition, the indirect relationship between mor- phology and speciation (Foley, 1991; Mayr, 1996; Tattersall and Criteria used to delineate species boundaries inevitably arise Schwartz, 2006) invalidates the original assumption, although from the Species Concept that is being applied (Quintyn, 2009). counterarguments allege that morphological differences should There are fundamental problems with creation of appropriate cri- suggest absence of reproductive isolation (Simpson, 1951; Wiens teria, mainly due to the occurrence of , with dif- and Servedio, 2000). Morphological criteria are, again, subjective ferent characteristics evolving at different rates (Mayr, 1996). and could ignore the evolutionary significance of species Taxonomy largely depends on morphological characteristics (Simpson, 1951). Nevertheless, such methods have some efficacy, (Simpson, 1961; Smith, 1994; Mayr, 1996), despite an indirect rela- as behaviour and morphology could be considered more relevant tionship between morphology and genetics (through reproductive to the production of species than genetic differences (Mallet, isolation) (Simpson, 1961; Mayr and Ashlock, 1991). This, accom- 2007), and morphology at least provides a clear method for species panied by inapplicability of many species ‘criteria’ to fossil samples demarcation (Mayr, 1996). (Tattersall, 1986) and small sample bases (Simpson, 1961), compli- cates the practice of species delineation, especially when consider- ing the Biological Species Concept. Subspecies Despite these inherent problems, certain criteria are regularly used, including: Subspecies can be defined as a group of organisms in which interbreeding with other subspecies occurs regularly (Simpson, – Reproductive isolation (Simpson, 1951; Harrison, 1998) which 1943), with each variant normally marked by significant morpho- can involve: logical differences (Keita et al., 2004). Genetically, subspecies exist  Genetic exclusivity (Harrison, 1998). as open systems (Dobzhansky, 1935) which may intergrade almost  Genotypic clusters (Harrison, 1998). unnoticeably (Mayr, 1964) or be separated by a migration barrier – Morphological divergence (Simpson, 1951) potentially leading (Livingstone and Dobzhansky, 1962). Four different definitions to: exist, summarised in Table 1. There is a trend towards the rejection  Autapomorphies (Nixon and Wheeler, 1990). of the term in scientific circles due to its ability to obscure the  Fixation of characters (Kimbel and Rak, 1993). more important relationships between members of populations (Gould, 1991), and application requires a minimum threshold of – Ecological distinctiveness (Simpson, 1951; Harrison, 1998). difference, as each population will have developed some genetic – Separate evolutionary identities and tendencies (Simpson, or morphological characteristic by which they could be distin- 1951; Harrison, 1998). guished from other groups (Templeton, 1999). The subspecies taxon is relatively more arbitrary than that of All species criteria require some level of qualitative, subjective species (Tetushkin, 2001), although Livingstone and Dobzhansky judgement (Sites and Marshall, 2004). For instance interbreeding, (1962) have argued that the naming and identification are subjec- where Mayr himself (Mayr, 1964), along with many others tive, whereas their existence is indisputable. Identification requires (Simpson, 1951; Harrison, 1998) acknowledges that interbreeding a large series of comparisons over the geographic range of the spe- may occur between populations that nevertheless retain their cies (Mayr, 1964), posing immediate problems for identification in genetic and morphological identities. This criterion cannot be used the archaeological record. Methods can be made more objective, in isolation (Mayr, 1964), and should be considered as a sufficient for example through the 75% rule where over 75% of a subspecies indication of species status, rather than a necessary criterion should be distinguishable by diagnostic characters (Mayr, 1964), (Balakrishnan, 2005). Genetic criteria have their associated issues, or more subjective, where contemporaneous subgroups in a larger with their validity under constant debate (Masters, 1993). Morpho- morphological group may be distinguishable (Simpson, 1943). logical criteria require an arbitrary level for a ‘sufficient’ level of There are no agreed criteria for distinguishing subspecies (Long divergence (Sites and Marshall, 2004), as does character fixation, and Kittles, 2003), with the main criterion being whether the where ‘true’ (100%) fixation is statistically impossible to prove (Wiens and Servedio, 2000). Table 1 Traditional taxonomy Four classes of subspecies definitions (Long and Kittles, 2003, p. 468). Class Definition Traditional taxonomy could be said to use primarily the Typo- Essentialist – Share a combination of derived traits logical Species Concept (Mayr, 1996; Boggs, 2001), based upon Lin- – Features more or less obscured by individual variations naeus’ own idea of species as static groups forming the lowest Taxonomic – Aggregate populations sharing phenotypic similarities category in his hierarchy (Mayr and Ashlock, 1991; Tattersall, – Inhabit geographic subdivision of range of the species – Differ taxonomically from other intraspecific populations 1992), marked by sharp discontinuity (Mayr and Ashlock, 1991) Population – Genetically differentiated and distinct Mendelian populations and representing divine origin (Mayr, 1964). This idea has been lar- – Consist of genetically differentiated individuals gely rejected by many researchers, owing to the problems that Lineage – A distinct evolutionary lineage within a species arise in polytypic species (Mayr and Ashlock, 1991). Instead, the – Genetically differentiated due to barriers to genetic exchange modern typological concept defines species as a ‘class of individu- over time – Historical continuity and genetic differentiation als sharing defining attributes’ (Boggs, 2001). It has the advantage S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 35 intraspecific variation is greater than interspecific variation among Table 2 groups (Long and Kittles, 2003). Five types of allopatry (Mayr et al., 1953). Contact Interbreeding Zone of Taxonomic contact classification Hybridisation 1 In contact – Intergradation/ Fairly wide – Same species interbreeding in – Subspecies status The definition of hybridisation that will be used is ‘‘interbreed- zone of contact dependent on degree of difference ing between individuals from genetically differentiated lineages 2 In contact – Interbreed Narrow – Same species over a wide range of taxonomic levels’’ (Jolly, 2001; Ackermann, completely in zone – Subspecies 2010). This process has been largely ignored or misunderstood, of contact possibly due to the nature of cladistics itself, which is inherently 3 In contact – Do not – Separate, full ineffective at identifying hybridisation (Holliday, 2003). However, interbreed freely species – Occasional Jolly (2001) has demonstrated how the acceptance of hybridisation hybrids can facilitate greater parsimony in cladistic phylogeny. Hybridisa- 4 In contact – No interbreeding – Full species tion is widespread in many groups of (Ackermann, 2010). – Reproductive Among primates, hybridisation occurs in Cercopithecidae (Cortés- isolation 5 Separated – No interbreeding Distributional – Unsure Ortiz et al., 2007), Papionins (Jolly, 2001; Arnold and Meyer, gap – Use morphology to 2006; Burrell et al., 2009), (Arnold and Meyer, 2006), infer taxonomic Orang-utans (Arnold and Meyer, 2006), (Ackermann and status Bishop, 2009), and (Arnold and Meyer, 2006). Con- – Preferable to treat sidering this widespread occurrence in the order and the as subspecies close genetic relationship between members of the Hominini (Holliday, 2003), the assumption that hybridisation did not occur within their original genome, and are therefore unlikely to be during hominin evolution is questionable and is likely to lead to lethal. If they are disadvantageous they may be removed by the inaccuracies in reconstruction. process of natural selection, meaning that they have a higher prob- Speciation is generally considered to be gradual process that ability of being advantageous. This in turn means that those genes can take between 2 and 4 Ma (Ackermann, 2010), with invi- which are mutually advantageous to both hybridising populations ability in mammals occurring at the end of this process could rapidly reach fixation (Jolly, 2001). In relation to Neander- (Fitzpatrick, 2004). Post-zygotic isolating mechanisms in mammals thal–AMH hybridisation, Jolly (2001) argued the issue of whether evolve over much longer timescales than behavioural or morpho- genetic evidence would survive in the face of the effects of later logical differentiation, meaning that if taxa meet after experiencing colonisation and genetic drift (Jolly, 2001): the recent studies of significant periods of isolation, reproduction could occur if not pre- the Neanderthal genome indicate that it may do so (Green et al., vented by pre-zygotic isolating mechanisms (Grant and Grant, 2010; Mendez et al., 2012; Wall et al., 2013). 1998; Holliday, 2006). A strongly relevant example is the high probability of gene exchange between human and ancestors up to 4 Ma after their initial divergence (Bower, 2006; Recognising hybridisation in the fossil record Patterson et al., 2006; but see Wakeley, 2008; Webster, 2009), and another is the documented hybridisation between Alouatta We have little knowledge of what a hybrid fossil would look like palliate and Alouatta pigra, species that diverged over 6 Ma (Ackermann, 2010), with Jolly (2001: 190) stressing the ‘‘vanish- (Arnold and Meyer, 2006). Holliday (2006) found that 172 out of ingly small’’ chances of recognising a Neanderthal–AMH hybrid. 328 documented occurrences of hybridisations between taxo- This position is the result of our lack of knowledge about the effect nomic species produce fertile, viable offspring. Considering the evi- of genetic introgression on the phenotype and the validity of the dence, later Homo sp. could be said to be members of a syngameon, assumption that such genes will be directly linked to morphology a term introduced by Lotsy (1925) referring to a larger group of (Jolly, 2001; Ackermann, 2010). The uncertainty is exacerbated by species capable of successful hybridisation (Holliday, 2006). the fact that the fossil evidence is likely to underestimate physical The BSC incorporates a certain level of hybridisation, demon- differences between specimens (‘Tattersall’s Law’) (Tattersall, strated by Mayr’s discussion of the five different kinds of allopatry 1993), and Jolly’s (2001) study of Papionin hybridisation empha- (shown in Table 2) in relation to interbreeding and taxonomic clas- sises the point. Beyond question we are restricted by the absence sification, which shows that separate species can be capable of of soft-tissue characteristics as well as the small samples available interbreeding in certain circumstances. The Neanderthal–AMH from an incomplete fossil record (Ackermann, 2010). interaction could be characterised as either condition 2, 3 or 4. In Jolly has emphasised the consequent need to rely on analogies, general, the conclusion that hybridisation between AMHs and for instance his direct analogy of the relationship between Hama- Neanderthals would indicate the conspecificity of these groups is dryas (Papio hamadryas) and Anubis (Papio anubis) baboons, which false (Ackermann, 2010) and a result of misdirected application produce natural hybrids after a divergence time of 600 Ka (Jolly, of the species concept (Hey et al., 2003; Arnold and Meyer, 2001). Such comparisons demonstrate that the assumed pattern 2006). The ‘issue’ of hybridisation does not exist, if one defines spe- of intermediate morphology is only one of many possible out- cies as lineages remaining cohesive despite occasional genetic comes, including: cryptic hybrids (those indistinguishable from exchange (Holliday, 2003). one of the parental taxa), transgressive hybrids (those showing Very low levels of interbreeding are required for favourable variation outside of the range of the parental taxa) and hybrids genes to spread between taxa (Barton, 2006) even if selection with phenotypes closer to one parental taxon rather than the other against hybrids occurs (Holliday, 2006) with the only requirement (Ackermann, 2010). Possible indicators could include intermediate being that at least some of the hybrids are partially viable and fer- characteristics, rare anomalies, or complicated patterns of synapo- tile (Jolly, 2001). In fact, genes introduced through hybridisation morphies and high levels of individual variability (Harvati et al., could have a higher probability of spreading through a population’s 2007; Ackermann and Bishop, 2009; Ackermann, 2010), although genome due to the nature of hybridisation. These genes, unlike these are features observed in hybrids of different genera and those arising through mutation, have been subject to selection may be less applicable to hominins. 36 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Evidence of Neanderthal–AMH hybrids AMH versus Neanderthals

The possibility of Neanderthal–AMH hybrids has long been AMH are more difficult to define in terms of their characteristic recognised, for instance with Dobzhansky’s (1944) proposition that morphology than Neanderthals (Wood and Richmond, 2000). the Mount Carmel specimens could indicate subspecific hybridisa- Table 4 lists some of the anatomical traits that can be used to dis- tion (Grant and Grant, 1998). Other examples analysed by Grant tinguish this morphospecies, yet most of these are defined in con- and Grant (1998) include some Krapina specimens, dated to trast to Neanderthals. One example is the uniquely derived nature 130 Ka, which display one of the aforementioned criteria of hybrid- of H. sapiens frontal bone morphology, which can be used to iden- isation: high occurrence of an unusual trait in the form of a rotated tify this group with high levels of accuracy (Arthreya, 2009). third premolar (36% in these specimens versus a normal rate of 6% Despite this, Arthreya (2009) has also commented that the high in Neanderthals and AMH). Three specimens from Qafzeh, along level of intraspecific variation leads to difficulties in describing with Skhul IV and also demonstrate dental anomalies the specific features that make this species so morphologically (Grant and Grant, 1998), and all occur in a supposed region of con- distinct. tact between H. sapiens and H. neanderthalensis, supporting their Tattersall (1986) has suggested that this high level of variation potential hybrid status. may in fact be interspecific: that H. sapiens could be an amalgam- There are multiple later examples of potential hybrids in Eur- ation of several separate species, with the ‘archaic’ and ‘anatomi- ope, mostly dating to the period when H. sapiens are known to cally modern’ groups representing two of these. H. sapiens may be entering this area, allowing for the creation of a hybrid zone. be defined by symplesiomorphic, not synapomorphic features The specific morphological characteristics are summarised in (Tattersall, 1992), and would therefore be cladistically unclassifi- Table 3, but here the focus is laid on a few key specimens. The first able. In the light of this possibility, the belief that H. sapiens is actu- is the well-known ‘hybrid child’ of Abrigo do Lagar Velho, dated to ally a subspecies could be seen as a gross misunderstanding of the 24.5 B.P. (Duarte et al., 1999). Despite displaying a mixture of fea- levels of intraspecific variation that can be contained within one tures that led some to conclude it has hybrid status (Duarte et al., species. 1999; Trinkaus and Duarte, 2000), Tattersall and Schwartz (1999) Neanderthals can be more easily defined and diagnosed using have emphasised that this F1-typical (first generation) mixture is their distinct morphological traits (Tattersall, 1992), as demon- not to be expected hundreds of generations after initial hybridisa- strated by the list of Neanderthal characteristics in Table 5. Gener- tion, proposed to have occurred around 30 ka (Trinkaus and ally Neanderthals are typified by increased robusticity and Duarte, 2000). More refined dating applications suggest that Nean- prominence of muscle attachment areas, with distinctive pelvis derthals disappeared from Iberia earlier than some radiocarbon and rib cage morphology, low crural and brachial indices, and a dates had indicated, perhaps as much as 40 ka (Higham et al., particular combination of cranial features including occipital ‘bun- 2006), but they do not affect the point that Lagar Velho is unlikely ning’ and midfacial prognathism. Neanderthals are associated with to belong with the first contacts. Holliday (2006) has also observed a specific combination of features and distinct general proportions that the existence of F1 hybrids in a hybrid zone is relatively rare, and relationships between cranial areas (Tattersall and Schwartz, which decreases the likelihood of discovering such a rare hybrid in 1998), with the craniofacial differentiation in comparison to the fossil record. AMH being considered by some to correspond to species status The Vindija specimens, dated to between 33 and 40 ka (Krings (Harvati et al., 2004). Tattersall (2007) has even stated that this et al., 2000; Higham et al., 2006) are generally accepted as H. nean- group is the most clearly demarcated extinct hominid group derthalensis, although some intermediate features could indicate a known as of yet, which would explain the frequent accurate differ- mixed ancestry (Ahern et al., 2002). Some have argued that this entiation of this group from other hominins by morphological would indicate the presence of hybridisation (Ahern et al., 2002), assessment (Harvati, 2003). whereas others have commented that individuals such as those This evidence would corroborate the classification of Neander- from Vindija could be Neanderthals independently evolving a mor- thals as a separate morphospecies (Harvati, 2003). Despite this, phology similar to that seen in the AMH trajectory (Delson et al., the question remains as to whether the listed traits are synapo- 2000). Such homoplasy could have arisen between the two lin- morphic, autapomorphic or symplesiomorphic. Tattersall (1992) eages due to phenotypic plasticity, where European Neanderthal and Kimbel (1991) have argued for the highly autapomorphic nat- morphology may have been responding to similar environmental ure of Neanderthals. Demonstrably derived features include pressures to AMH. aspects of the bony labyrinth (Spoor et al., 2003), general facial morphology (Rak, 1993), and the mandibular fourth premolar

(P4)(Bailey, 2002; Bailey and Lynch, 2005). In these three cases Morphological assessment AMH bear closer resemblance to than Neanderthals do. The case is even stronger for the derived nature of Neanderthal As has been noted, morphology is the most common elbow morphology, with AMH morphology being more similar to method for taxonomic assignation in hominin palaeontology. that of the (Yokley and Churchill, 2006). To reduce or eliminate subjectivity, comparative methods are Neanderthals inevitably retain some symplesiomorphic fea- employed to define levels of expected intraspecific and inter- tures, for instance large supraorbital tori, a low cranial vault specific variation in morphological traits of living species (Santa Luca, 1978) and aspects of the pelvis (Rak, 1993). These (Mayr and Ashlock, 1991; Tattersall, 1986; Harvati, 2003). are not unexpected, and evidence evolutionary relationships such Although this method is more complicated and results in less as those between Neanderthals and the Steinheim and Sima de certain conclusions, it is the only relatively objective and satis- los Huesos specimens (Wood and Richmond, 2000; Tattersall, factory method that can be applied to morphology. There is a 2007). The characteristics shared with AMH merely demonstrate clear lack of a closely-related out-group for comparative analy- their relationship as sister taxa and the fact that they were gener- ses. Chimpanzees, our closest living relative, do not represent a ally synchronic and sympatric groups (Holliday, 2003), and there- valid candidate, due to the large evolutionary gap between fore could be homoplastic (Stringer and Andrews, 1988). This point them and hominins and the possibility that they may have is also indicated by the large amount of intraspecific variation undergone a different pattern of morphological differentiation found in both groups (Tattersall and Schwartz, 2006; Arthreya, (Harvati, 2003). 2009), which vary over a wide range, with minimal overlap S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 37

(Harvati, 2003) yet maintain distinctly different means (Tattersall which could affect estimates of genetic diversity (Briggs et al., and Schwartz, 1998). Comparisons with other closely-related 2009), yet the recent application of a high coverage method (Max mammalian species show that minimal differentiation and large Planck Institute for Evolutionary , 2013) also overlap in hard-tissue characteristics are the norm (Tattersall, employed by Meyer et al. (2012) for material, could 1986; Tattersall and Schwartz, 1998), with differences between resolve this issue in the future. subspecies of primates being comparatively tiny (Tattersall, 1986). As in morphological analysis, single genetic synapomorphies The morphological evidence leads to one conclusion, that Nean- can theoretically be used to define phylogenetic relationships, derthals and AMH represent distinct species. Neanderthals in par- but this is only possible in rare situations (Knight, 2003), necessi- ticular are a distinctive, cohesive evolutionary group (Santa Luca, tating in-depth study to reveal interactions between Neanderthals 1978; Tattersall and Schwartz, 1998). The most important point and AMH. The identification of hybridisation through DNA analysis to note is the clear hiatus between the Neanderthal and AMH mor- is theoretically possible, with hybrid DNA showing different diver- phologies (Santa Luca, 1978). The comparative difference between gence times in comparable regions of the genome (Lalueza-Fox Neanderthals and AMH is at least as great as that between closely- et al., 2012), yet can be complicated by numerous factors, which related extant species (Tattersall, 1986), and in the case of cranio- are treated here briefly. dental evidence, larger (Tattersall, 1992). Harvati’s comparison of intraspecific and interspecific variation with chimpanzee species Mitochondrial DNA evidence has led to a similar conclusion: the difference between Neander- thals and AMH is greater than AMH intraspecific variation, and Early genetic studies were based on the analysis of mitochon- greater than the distance between paniscus and Pan troglodytes drial DNA (mtDNA). MtDNA is particularly useful for ancient (Harvati, 2003). As the majority of morphological change in a line- DNA studies due to its relative abundance and increased likelihood age is expected to arise after the true speciation event, even incip- of retrieval (Endicott et al., 2010), as well as the fact that it is ient Neanderthal features would be sufficient to conclude separate maternally inherited (Giles et al., 1980) and thus non-recombining species status (Rak, 1993). (Green et al., 2008; Lalueza-Fox et al., 2012). MtDNA from no less than 22 Neanderthals (Krings et al., 1999; Scholz et al., 2000; Ovchinnikov et al., 2000; Schmitz et al., 2002; Beauval et al., Genetic evidence 2005; Lalueza-Fox et al., 2005, 2006; Caramelli et al., 2006; Noonan et al., 2006; Orlando et al., 2006; Serre and Pääbo, 2006; Enormous progress has been made in the last twenty years in Green et al., 2008; Briggs et al., 2009), and 8 AMHs (Scholz et al., the recovery of genetic evidence from bone (Pääbo, 2003; Green 2000; Caramelli et al., 2003; Serre et al., 2004; Pettitt, 2011) has et al., 2006, 2010; Valdiosera et al., 2006; Meyer et al., 2012; been analysed. Most compare Neanderthal evidence with modern Dabney et al., 2013), considerably reshaping views of human evo- mtDNA, but signals of admixture may have been affected by later lution through the last half million years. There remain numerous genetic bottlenecks and drift, necessitating comparison with pre- problems associated with DNA studies into Neanderthal introgres- historic AMH DNA. sion, although it must be admitted that very rapid progress in Such studies conclude that Neanderthal DNA clusters to the development of techniques will much reduce these. Obvious exclusion of modern humans (Krings et al., 2000; Knight, 2003), sources of error include contamination from modern human with the overall difference between the two populations being DNA, which is pervasive in archaeological remains (Serre et al., three times as great as the intraspecific mtDNA variation for mod- 2004; Serre and Pääbo, 2006), and exacerbated by the damaged ern humans (O’Rourke et al., 2000; Tetushkin, 2001) and half of nature and small samples of Neanderthal DNA (Green et al., that between modern humans and chimpanzees (O’Rourke et al., 2009). This difficulty is coupled with the overwhelming similarity 2000). This finding leads to the conclusion that no introgression of Neanderthal and AMH DNA (Serre and Pääbo, 2006; Green et al., occurred (Tetushkin, 2001), supported by the lack of any direct evi- 2008, 2009), often leading to AMH-like DNA sequences being taken dence of introgressed genes. as evidence of contamination rather than introgression (Serre et al., If the absence of evidence of introgression is a true reflection of 2004). the prehistoric situation, it would limit the possible amount of DNA analyses depend on estimates of the population size of the admixture that occurred (Krings et al., 2006), with maximum esti- invading H. sapiens population (Forhan et al., 2008) and genetic mates ranging from 0.1% to 25% (Forhan et al., 2008) and minimum diversity, both of which may have been variable and are difficult estimates of 0 (Ghirotto et al., 2011). Yet there are many issues to estimate (Wall, 2000). There is a high probability that both associated with mtDNA analyses, including frequent introgression Neanderthals (Orlando et al., 2006; Dalén et al., 2012) and AMH of mtDNA across species boundaries (Barton, 2006), dependencies (Loogväli et al., 2009; Wall et al., 2009) underwent significant pop- on estimates of mutation rates (Hawks, 2006), and questionable ulation and genetic bottlenecks, which could explain the reduced claims of the selective neutrality of mtDNA (Nordberg, 1998; genetic diversity of later Neanderthals (Krings et al., 2000; Serre Hawks, 2006). A negative consequence of the maternal inheritance and Pääbo, 2006), although the results of the study of Lalueza- of mtDNA is that such sequences cannot reveal the entire evolu- Fox et al. (2005) would contradict this bottleneck hypothesis. tionary history of a population (Templeton, 2005), meaning that Alves et al. (2012) have even suggested that admixture would have nuclear DNA analyses are required to corroborate the conclusion a significant effect on such estimates of AMH demography. of an absence of Neanderthal–AMH admixture (Beerli and Issues also exist in the data sets used, as most comparative AMH Edwards, 2002; Lalueza-Fox et al., 2012). DNA is from modern individuals, yet later effects such as drift and genetic ‘swamping’ could eliminate traces of earlier introgression Nuclear DNA evidence (Serre and Pääbo, 2006), so that larger samples of Upper Palaeolith- ic AMH DNA would be required for gaining a more balanced pic- The main results of the Neanderthal genome study were first ture (Nordberg, 1998; Serre et al., 2004). It is unlikely that we published by Green et al. (2010), who used a new measure, the D shall retrieve sufficient DNA from the common ancestral species statistic, and concluded that introgression of Neanderthal genes (Lindahl, 1997; Krings et al., 2006) which limits us to estimations into the AMH genome of between 1.3% and 2.7% must have of the symplesiomorphic genome. Early samples were of small occurred due to the fact that Neanderthal DNA was closer to DNA fragments from few individuals (Serre and Pääbo, 2006), that of non-Africans than to that of Africans. They argue that, as 38 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Table 3 Review of possible Neanderthal–AMH hybrids.

Site Date H. neanderthalensis features H. sapiens features Intermediate/anomalous Taxonomic features assignation Cioclovina, 29–210 kya (33.2– – Supraorbital torih,o – Supraorbital tori not H. sapiensh,q Romania 33.8 kya BP cal)q Suprainiac fossap,q continuousq – Nuchal torusp,q – Superior nuchal lines (position – External occipital and size)q protuberanceq – High, vertically rising frontal – Occipital ‘hemi-bun’p squamah – Prominent glabellah – High and rounded cranial vaulth,q – No anterior mastoid tubercleh – Small juxtamastoid eminenceh,q – Narrow digastrics fossah – Well-developed superior nuchal lineh – No suprainiac fossah,q – Laterally and inferiorly prominent mastoid processq – Coronal outlineq Abrigo do Lagar 25.6 kyaf – Juxtamastoid eminencei – Development of ‘‘chin’’f,r – Size of juxtamastoid – Hybridf,r i f f Velho, Portugal –I2 shovelling –I2 breadth process – Possible i f f k – Suprainiac fossa – Breadths of I2 versus Ms – Size of mastoid process hybrid? – Juxtamastoid eminencef – Anteromedial position of radial – H. sapiensc – Posterior retreat of tuberosityf mandibular symphysisf,i – Little lateral curvature of the – Dental maturational patternc radiusf – Anterior symphyseal – Small front teethr configuration of the mandiblef – Short facer – Femoral midshaft – Minimal brow developmentr circumference versus lengthf – Narrow anterior pelvisr – Proximal humeral diaphyseal morphologyf – Strongly developed pectoral musclesf – Short, stout legsr – Backwards sloping of mandibler – Limb segment proportionso Mladecˇ 1 and 2 31 kyat – Pronounced occipital ‘bun’t – High foreheadt – H. sapiens?d,t (females) – Distinctive nuchal areat – Reduced browst – Large juxtamastoid – Small facial dimensionst eminencesp Mladecˇ 3 (infant) 31 kyat – Thick, well-developed medial – Shape of orbitj – Nuchal plane lengthj Hybridj brow ridgesj – Degree of frontal vaultingj – Occipital breadthj – Prominent glabellaj – Antero-superior orientation of – Strongly developed occipital the external auditory meatusj bunj,p – Strongly concave glenoid fossaj – Low occipital heightj – Post-glenoid tuberclej – Lambdoid flatteningj – Flat squamous temporalj – Short occipital plane lengthj – Short and low temporal bonej – Prominent juxtamastoid eminencej Mladecˇ 6, 7 and 9 31 kyat – Small mastoid processesg – Supraorbital projectiong – Vertical heightg – Possible (males) – Lateral profileg – Supraorbital sulcusg – Supraorbital torus hybrid?g – Elliptical suprainiac fossaeg – Divergence of the temporal lineg structureg – Not hybridd – Shallow groove on inferior – Parietal thicknessg – Occipital (biasterionic) nasal marginsg – Occipital plane lengthg breadthg – Cranial height/length indexg – Mandibular fossag – Cranial breadthg – Strongly curved frontal boned – Nasion projectiong – Glabella projectiong – ‘Square’ parietal bonesg – Occipitomastoid crestg Pesßtera cu Oase, 34–36 kyas – Unilateral bridging of – Mesial mental foramens – Lingual bridging of the H. sapienss Oase 1 mandibular forameno – Narrow lateral corpuss mandibular foramens (mandible) – Absence of retromolar spaces – Distal molar megadontias – Symmetrical mandibular incisuress – Lateral incisures crests – Small superior medial pterygoid tubercles S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 39

Table 3 (continued)

Site Date H. neanderthalensis features H. sapiens features Intermediate/anomalous Taxonomic features assignation Pesßtera cu 36 kyal – Sagittal frontal arc (long and – Overall cranial proportionsl – Unsure, possible Oase,Oase 2 flat) l,p – Subrectangular orbitsl hybridl (cranium) – Large juxtamastoid eminencel – Infraorbital regions – – Large buccolingual and pronounced canine fossael mesiodistal diameters of – Modest superciliary archesl molarsl – Narrow nasal aperturel – Molar size progressionl – No anterior mastoid tuberclel – Occipital ‘hemi-bun’p – High, rounded parietal regionl,p – Pentagonal contour in norma occipitalisl Pestera Muierii, 36 ky BP (cal)m – Frontal curvature of the – Small superciliary archesm – Marked projection of the Possible hybrida,m Muierii 1 neurocranial vaultm – Deep canine fossaem occipital bunm – Shallow transverse suprainiac – Anterior zygomatic roots above m c fossa M12 – Median nuchal torusm – Modest nasal aperture breadthm – Lacks retromolar spacem – Dentitionm – High coronoid processesm – Scapulam – Asymmetrical notchesm,p – Breadth/height index of scapular glenoid fossam – Moderately low frontal arc of craniumm – Occipital ‘bun’p Vindija, G1 29–210 kyab – Reduced midfacial – H. prognathismb neanderthalensis?b – Reduced nasal breadthb – Possible hybridb – Thinner cranial vaultsb – Incipient chinsb – Reduction and shape changes in supraorbital torusb – Scapular glenoid fossae

a Ackermann (2010). b Ahern et al. (2002). c Bayle et al. (2010). d Bräuer et al. (2006). e Di Vincenzo et al. (2012). f Duarte et al. (1999). g Frayer et al. (2006). h Harvati et al. (2007). i Holliday (2003). j Minugh-Purvis et al. (2006). k Quintyn (2009). l Rougier et al. (2007). m Soficaru et al. (2006). n Soficaru et al. (2007). o Trinkaus (2005). p Trinkaus (2007). q Trinkaus and Duarte (2000). r Trinkaus et al. (2003). s Wild et al. (2005). t Wolpoff et al. (2006).

Neanderthals are equally related to Chinese, Papua New Guineans statistic would be confounded by such a population history, but and French, introgression must have occurred in the Middle East. conclude that admixture is a more parsimonious possibility than Neves and Serva (2011) subsequently argued that the results need population substructure for the results of Green et al., and con- to be replicated before they can be accepted, preferably with larger clude that tests could be used to eliminate substructure as an samples of Neanderthal and Upper Palaeolithic nDNA, in view of the explanation. Similarly, Lohse and Frantz (2013) used a maximum contradictory mtDNA evidence (Tetushkin, 2001; Krings et al., likelihood method to reject population substructure as a cause of 2006). Nuclear DNA from the Vindija specimens had been analysed the genetic signatures found. Sankararaman et al. (2012) have previously (see Serre et al., 2004; Noonan et al., 2006), however made the lucid argument that, if interbreeding did occur after studies failed to find evidence of introgression. Neanderthals and AMH diverged, then genes would have been An alternative explanation for Green et al.’s results might be exchanged after 100 ka. If the substructure argument was valid, that of ancient population substructure in AMH populations before the date of the last genetic exchange would be closer to the date they left Africa (Lalueza-Fox et al., 2012), with the African subpop- of common ancestry, around 230 ka (Sankararaman et al., 2012). ulation that later gave rise to the dispersing AMHs sharing a longer As can be seen, there are ways to eliminate the explanation of sub- ancestry with Neanderthals (Ghirotto et al., 2011). This point has structure in this debate. been acknowledged by Green et al. (2010) and supported by the Many studies published since Green et al.’s (2010) paper have research of Wall et al. (2009) and analysis of the Xp21.1 gene shown supporting evidence of introgression, frequently using (Garrigan et al., 2005). Durand et al. (2011) suggested that the D- divergent haplotypes (e.g. Abi-Rached et al., 2011) or patterns of 40 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Table 4 Table 5 List of AMH morphological characteristics. List of Neanderthal morphological characteristics.

Location Trait Location Trait Cranial Calvarium Globular braincaseg Cranial traits Calvarium Smoothly rounded cranial profile from rear traits Short, high craniumf view (‘en bombe’)g,m,n,p Long, high parietal archf Lower cranial vaultd Parietal arch – narrow inferiorly, broad Shorter, wider occipital planed superiorlyf Suprainiac fossae,g,j,m,o,p High frontal archf,g Rounded, laterally projecting parietal boner Rounder frontal bonesa Lambdoid flatteningo Thin bones of cranial vaulte Anteriorly placed lambdae Upper facial Discontinuous supraorbital torif Occipital ‘bun’ (posteriorly projecting region Reduction of supraorbital toria,e,g occipital)o,q,r Curved occipital bonef,f Horizontal occipital torus of uniform Orthognathye thicknessj,m Nasal region Shorter nasion bregma chorda Occipital torus restricted to central part of Mandible Mental eminence (chin)f,g occipital bonej,m Thin bone of mandibular bodye Angling along anterior squamosal suturen Dental Anterior teeth Canine fossag Pronounced juxtamastoid eminenceg b m Postcanines Perfect oval shape of mandibular P4 Large juxtamastoid crest b d Wide lingual crown of mandibular P4 Smaller mastoid process Simplified occlusal morphologyg Rounded mastoid protuberancej,m Reduced crownsc,g Occipitomastoid process P mastoid process j,o Reduced root sizec Upper facial Thick, double arched supraorbital torio,q,r Symmetrical lingual crown contourg region Supraorbital tori continuous across the Absence of transverse crestg glabellao Absence of accessory ridges and fissuresg Inferomedially truncated orbitsn,p Reduction in number of cusps and rootsg Retreating zygomatic profilem,n,r Absent or reduced metaconid forming a Long, thin zygomatic archesp lingual shelfg Pronounced midfacial prognathismd,g,m,r Postcranial Trunk Narrow trunkg Nasal region Well-developed medial projection of internal Limbs Elongated distal limbsg nasal margink Long limbs relative to trunkg Swelling of lateral nasal cavitywallk Small humeral bi-epicondylar breadthsh Capacious nasal aperturem,o Pelvis Short, stout pubic ramus with rounded cross- Large nasal fossao sectiond Lateral expansion of the frontal sinuseso Narrow pelvisg Projecting nasal bonesm General Low body mass relative to statureg Maxilla Underdeveloped mental eminenceo,r Loss of robusticitye,g Lack of ossified groove over lacrimal groovek Narrow lower facen,o a Arthreya (2009). Mandible Sigmoid notch crests terminate close to lateral b Bailey and Lynch (2005). ends of condylesn c Kupczik and Hublin (2010). Sigmoid notches deepest in front of low-set d Rak (1990). condylen,p e Stringer and Andrews (1988). Obliquely truncated gonial anglesn f Tattersall (1992). Inferior, lateral position of articular eminenced g Wood and Richmond (2000). Mental foramen under first mandibular molarr h Yokley and Churchill (2006). Thin symphyseal bonep Cranial base Wide sphenoid anglem Highly pneumatised petrosal bonen,p linkage disequilibrium (e.g. Hammer et al., 2011) to infer admix- Long, narrow, ovoid foramen magnumn,p ture with ancient populations. We now have a much more broadly Pronounced juxtamastoid eminenceg m based view of our genetic ancestry; Mendez et al.’s (2012) study Large juxtamastoid crest Smaller mastoid processd shows that the derived STAT2 haplotype, a potential candidate of Rounded mastoid protuberancej,m introgression, was ten times more likely to be found in Papua Occipitomastoid process P mastoid processj,o New Guineans than in other groups, Wall et al. (2013) argue that Bony Anterior Relatively small and narrowl l Neanderthal genes are more prevalent in East Asians than - labyrinth semicircular Narrow in width relative to height arc ans, while Hammer et al. (2011) believe that their genetic analysis Posterior Relatively smalll is indicative of introgression with a previously unknown transi- semicircular Positioned more inferiorly relative to lateral tional hominid from Central Africa. In addition to these geographic canal arc canal placel regions, we now have potential evidence of secondary introgres- Lateral Absolutely and relatively largel sion (i.e. from an AMH population carrying introgressed genes) in semicircular arc North Africa (Sánchez-Quinto et al., 2012) and (Wall Ampular line More vertically alignedl et al., 2013). A new interpretation is that our African ancestry Dental Anterior Broad anterior teetha,h,m,r was mosaic in nature, with potentially multiple as yet un-defined teeth Shovelled incisorsa,f,h,r a hominins contributing to our modern genome (Hammer et al., Prominent lingual tubercles a,f 2011; Stringer, 2012). Comparisons can be drawn with the idea Labial convexity Postcanines Relatively thin enamelh of population subdivision, as these hominins may represent the Retromolar spaceg,m,o,q,r beginnings of subspecies division, while being insufficiently differ- Complex occlusal surfacesa,n,p entiated to warrant full species status. Mid-trigonid crest more frequenta,f The assumption that divergent haplotypes or specific patterns Inwardly sloping centroconids and centroconesn of linkage disequilibrium are indicative of introgression needs to Extra fissures, ridges and lingual crestsa be validated. Such signals could arise from other processes such Larger crown baseh as fixation of genes or incomplete lineage sorting (Alves et al., S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 41

Table 5 (continued) 2012), and do not exclude the possibility of ancestry. The use of chimpanzee DNA as an ancestral comparison merely shows that Location Trait the derived states could have evolved any time after the diver- h,r Large root canals gence with our common ancestor (Lowery et al., 2013). A recent Longer rootsh Enlarged pulp chambers (‘taurodontism’)a,f,h study has demonstrated the plausibility of genetic drift and demic Mandibular Strong, continuous transverse cresta,b diffusion in creating a cline of introgression from Europe to Asia, P4 Well-developed, medially placed metaconida which could otherwise be interpreted as differing levels of hybrid- a,b Truncated mesiolinguallobe isation (Lowery et al., 2013). It is doubtful that we will be able to Narrow lingual crownb Asymmetrical crown shapea,b overcome the inherent assumptions of modern genetic studies Postcranial Trunk Large dorsal sulcus on scapulaem without the retrieval of DNA from specimens ancestral to both Long scapulaen Neanderthals and AMH. With luck this could be possible, given n Expanded rotator cuff attachments the successful retrieval of DNA of a cave bear (Ursus deningeri) from Well-marked muscle attachments alongs Sima de los Huesos, dated to 400 ka (Valdiosera et al., 2006; capulaer Long, narrow glenoid fossaen Dabney et al., 2013), but future research would be constrained Long clavicles with flattened shaftsn,q,r by the decreasing size of DNA fragments which can be retrieved Flaring iliac bladesn as the age of the specimen increases (Valdiosera et al., 2006). Ribcage is narrow at top and flares out and In addition to the Neanderthal draft genome, we now have downn Broad ribcageq,r genetic evidence from the phalanx found in , dating Mobile vertebral column set against inferiorly to 40 ka (Krause et al., 2010). It has been suggested that this spec- placed sacrumn imen represents a sister group to the Neanderthals, splitting off n Reduced vertical length of the waist around 465 ka (Krause et al., 2010). Original analysis of recovered m Limbs Pronounced radial curvature nuclear DNA suggested introgression with Melanesians at a level of Thick corticesn Restricted medullary cavitiesn approximately 4.5%, which is presumed to have taken place after Expanded articular surfacesn the admixture event between Neanderthals and AMH (Reich Robust limb bonesq,r et al., 2010). A recent study was able to produce a high coverage r Well-developed muscle attachments sequence from the same specimen (Meyer et al., 2012), a finding Short distal extremities resulting in low brachial and crural indicesq,r which has clear implications for the future of the hybridisation Bowing of femorar debate. With evidence of such a complicated genetic history of Low humeral torsion angles our species, most probably fraught with extensive reticulation over Narrow humeral deltoid tuberositiesc a significant period of time, it is clear that the question of Neander- c Robust humeral diaphysis thal–AMH hybridisation is far more intricate than previously Large, transversally humeral headsc Enlarged epiphyses with large articular anticipated. surfacesc Large olecranon fossaec,s Models of admixture Humeral medial and lateral pillars that are distodorsally smalls m,r Some have attempted to model the levels of admixture that Hands and Flattened first carpometacarpal joint feet Elongated polluxm could result in such seemingly contradictory evidence between Long pollical distal phalanxr mtDNA and nuclear DNA. For instance, Currat and Excoffier Large carpal tunnelsn (2004) concluded a maximum estimate of 34–120 admixture Expanded pollical and ulnar distal phalangeal events in the entire 12.5 ka estimated period of admixture, corre- tuberositiesn Accentuated muscle attachment areasn sponding with a maximum level of introgression of Neanderthal Robusticityr genes at 0.02–0.09%. This estimate does not match the results of Pelvis Wide pelvisr Green et al. (2010), although a later Neolithic expansion of H. sapi- i,m,n,r Long, plate-like superior pubic ramus ens could have led to a decrease in the existing signal, as could Anteriorly placed sacrumr dilution effects and genetic drift (Currat and Excoffier, 2004). A Anteriorly placed pelvic inleti Triangular shaped ishiopubic regioni later model estimated interbreeding success rates to be below Obtuse subpubic anglei 2%, which would result in low levels of introgression in mtDNA evi- Internal obturator groove encroaches upon dence (Currat and Excoffier, 2011). This would predict the disparity i ischial tuberosity between the mtDNA and nuclear DNA evidence, but is dependent a Bailey (2002). on the accuracy of the estimates of the period of admixture. b Bailey and Lynch (2005). Another relevant model is that of Belle et al. (2009), who used c Churchill and Smith (2000). coalescent theory to compare Neanderthal, AMH and modern d Harvati (2003). e Harvati et al. (2007). human information with simulated genealogies. This work f Hershkovitz et al. (2011). resulted in a best estimate of no admixture between Upper Palae- g Holliday (2003). olithic populations, with a maximum level of 0.001% interbreeding h Kupczik and Hublin (2010). per generation. There are thus obvious incongruities in the predic- i Rak (1990). tions of different models which could negate their efficacy in this j Santa Luca (1978). k Schwartz and Tattersall (1996). debate. For instance Hawks and Wolpoff (2006) found that the null l Spoor et al. (2003). hypothesis of no introgression could not be rejected, but that the m Tattersall (1992). variation found was within the expected range for a subpopulation n Tattersall (2007). connected by gene flow, thus refuting the assignation of Neander- o Tattersall and Schwartz (1998). p thals to a separate species. Tattersall and Schwartz (2006). q Wood and Lonergan (2008). A recent model developed by Eriksson and Manica (2012) r Wood and Richmond (2000). explored the effect of ancient population substructure. Their model s Yokley and Churchill (2006). fitted the genetic results more closely than Green et al.’s proposal, again showing that we cannot accept the conclusion of hybridisation 42 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Table 6 Summary of mtDNA analyses of Neanderthals and AMH.

Age (kya) Results Reference Neanderthals La Chapelle aux Saints No introgression Serre and Pääbo (2006) Engis 2 No introgression Serre and Pääbo (2006) Feldhofer 1 40 No introgression Briggs et al. (2009) Feldhofer 2 40 No introgression Briggs et al. (2009) Krapina 110–100 No introgression Scholz et al. (2000) Mezmaiskaya 1 60–70 No introgression Briggs et al. (2009) Mezmaiskaya 2 41 No introgression Briggs et al. (2009) Mezmaiskaya? 29.2 No introgression Ovchinnikov et al. (2000) Monte Lessini 50 No introgression Caramelli et al. (2006) Neandertal NN 1 40 No introgression Krings et al. (1999), Schmitz et al. (2002) La Rochers de Villenueve (RdV1) 40.7 No introgression Beauval et al. (2005) Scladina cave 100 No introgression Orlando et al. (2006) El Sídron 44 No introgression Lalueza-Fox et al. (2006) El Sídron 441 40 No introgression Lalueza-Fox et al. (2005) El Sídron 1253 39 No introgression Briggs et al. (2009) Vindija No introgression Krings et al. (2000) Vindija (?) 38 No introgression Noonan et al. (2006) Vindija 33.16 38.3 No introgression Green et al. (2008) Vindija 33.25 >38 No introgression Briggs et al. (2009) Vindija 77 No introgression Serre and Pääbo (2006) Vindija 80 38.3 No introgression Serre and Pääbo (2006) Warendorf-Neuwarendorf >50 No introgression Scholz et al. (2000) Anatomically Modern Humans (AMH) Paglicci 12 24.72 No introgression Caramelli et al. (2003) Paglicci 25 23 No introgression Caramelli et al. (2003) Mladecˇ 25c No introgression Serre et al. (2004) Mladecˇ 2 32.3 No introgression Serre et al. (2004)Pettitt (2011) Cro-Magnon No introgression Serre et al. (2004) Abri Pataud No introgression Serre et al. (2004) La Madeleine No introgression Serre et al. (2004) Stetten I 35 No introgression Scholz et al. (2000) until we have ruled out other phenomena. However, a major prob- lem arises in the dependence of models such as this on estimates Table 7 Some of the molecular divergence estimates for Neanderthals and AMH. of the time period of hybridisation. The timing has a significant effect on expected levels and direction of introgression (Currat and Divergence Calibration: References Type of Excoffier, 2011). Speciation is not instantaneous, often taking 2– estimate homo–chimp DNA used (Kya) split (Mya) 4 ma to reach full behavioural, ecological or reproductive isolation. Therefore, the probability of reticulation should increase as we 407 6–7 Endicott et al. (2010) mtDNA 435 6.5–7.5 Endicott et al. (2010) mtDNA approach the point of cladogenesis. 465 (317–741) 4–5 Krings et al. (1999) mtDNA Estimates of the time of the Neanderthal–AMH divergence, sum- 461–825 4.7–8.4 Green et al. (2006) mtDNA marised in Table 7, cover a wide range of 407–825 kya. Comparably, 516 (465–569) 6.5 Green et al. (2006) nDNA Endicott et al. (2010) dated the population divergence (as opposed 550–690 4–5 Krings et al. (2006) mtDNA to the genetic divergence) of the two to 343–373 kya. The calibra- 631–789 4–5 Beerli and Edwards mtDNA (2002) tion point of the human–chimpanzee divergence is the main con- 660 (520–800) 6–8 Green et al. (2008) mtDNA tributor to the wide range seen in Table 6, as this could date 825 6.5 Green et al. (2010) nDNA and anywhere between 6 and 11 ma (Patterson et al., 2006; Jensen- mtDNA Seaman and Hooper-Boyd, 2008; Langergraber et al., 2013). Error is compounded by the need to use additional calibration points for this divergence, normally the split of the Old World Monkeys (37–23 Mya) (Jensen-Seaman and Hooper-Boyd, 2008) or that of there continues to be considerable debate as to when this element the Orang-utans from African (23–13 Mya) (Holmes et al., was introduced. When publishing the draft Neanderthal genome 1989; Patterson et al., 2006). Consequently, the human–chimpan- sequence, Green et al. (2010) admitted the possibility that this zee split is not well-suited for use as a calibration point (Endicott apparent introgression could in fact be due to ancestral population and Ho, 2008), and more accurate results could be obtained by structure (see also Eriksson and Manica, 2012). The population the use of multiple internal archaeological or biogeographic calibra- structure argument explains the fact that non-Africans share more tion points within the Homo lineage (Pulquério and Nichols, 2007; genetic material with Neanderthals than do sub-Saharan Africans Endicott and Ho, 2008). Methods applying recent estimates of sub- by postulating an ancestral geographical division between sub- stitution rates could question the use of fossil calibration, with Saharan and North-eastern Africans. If this division predated the obtained dates being considerably older than those from fossil cal- departure of Neanderthal ancestors from North-eastern Africa, ibration studies (Fu et al., 2013). Until we can gain more reliable and persisted at least until the first migrations of H. sapiens out estimates for the divergence time of Neanderthals and AMH that of East Africa, then it could account for the genetic affinities of are not accompanied by extremely wide, compounded error mar- non-African populations and Neanderthals without the need to gins, assessment of the time of hybridisation and its significance posit subsequent interbreeding (see e.g. Sankararaman et al., will remain very difficult. 2012). However, a number of recent studies have cast doubt on Although it is now widely accepted that non-African humans the population structure argument, arguing that the sharing of inherit around 1–3% of their genomes from Neanderthal ancestors alleles is due at least partially to recent admixture (Prufer et al., (e.g. Green et al., 2010; Prufer et al., 2014; Vernot and Akey, 2014), 2014; Sankararaman et al., 2012; Yang et al., 2012; Wall et al., S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 43

2013; Vernot and Akey, 2014). Sankararaman et al. (2012) go (2010) argue for interbreeding at an earlier stage (>60 ka), Currat beyond these tentative conclusions, arguing that some inbreeding and Excoffier (2011) have aimed to explain the data in terms of occurred between H. sapiens and Neanderthals more recently than more recent contacts in Europe. While this debate remains unre- 86 ka. The idea of minor gene flow events between as many as four solved, we cannot make general conclusions regarding the signifi- hominin groups in the Late (H. sapiens, H. neanderthal- cance of the interbreeding, but it remains clear that it was not ensis, , and a fourth, as yet unnamed group (Prufer et al., sufficient to affect Neanderthal’s species status. 2014)) is consistent with current data; however, such data remain The use of genetic evidence to decide taxonomic status relates insufficient to cast doubt on the integrity of H. neanderthalensis as a most comfortably to the Biological Species Concept (BSC). The logic species, particularly whilst the extent of allele sharing that is due behind this has been demonstrated by Ferguson (2002) (see Fig. 2), to ancestral population structure remains unknown. and is dependent on a sequence of assumptions. Use of genetics is also theory-based, and dependent on unproved presumptions. Therefore it will always have to be supplemented by ecological DNA analyses and their status and behavioural evidence (Ferguson, 2002), which may be more difficult to access. Problems also arise from the previously men- There are clear discrepancies between the different sets of tioned misapplication of the criterion of reproductive isolation, genetic evidence, which could be partly explained by complicated and the fact that relatively few genetic changes may be required demographic and genetic processes in the evolutionary history of for reproductive isolation through pre-zygotic (e.g. behavioural, the two groups mainly in question. It has been stated that it would ecological, physical) isolating mechanisms (Ferguson, 2002), which be impossible to disprove interbreeding from absence of evidence are the main candidate for the barrier limiting interbreeding of introgressed genes, as this absence could also result from low between Neanderthals and AMH (Klein, 2008). Such mechanisms levels of interbreeding (Wall, 2000; Pääbo, 2003; Ghirotto et al., could include sociocultural differences (Holliday, 2006), social 2011). Therefore the existence of some evidence of admixture is avoidance or assortative mating (Barton and Riel-Salvatore, 2012) noteworthy, even in the form of low levels of introgression. While and low survival of hybrids (Currat and Excoffier, 2011; Ghirotto the low rates could be explained by possible pre-zygotic preventa- et al., 2011). All of these are more porous than true post-zygotic tive mechanisms to interbreeding (Currat and Excoffier, 2011), isolating mechanisms (reproductive isolation caused by genetic Templeton (2005) has commented that levels of gene flow are bio- differences) (Garrigan and Kingan, 2007), meaning that limited logically significant if the migration rate multiplied by population introgression, as evidenced by genetic studies, could occur under size is greater than 1, implying that Green et al.’s (2010) prediction such a model. of 1.3–2.7% gene flow would be significant regardless of population The discrepancies between recent nuclear studies and previous size. mitochondrial evidence can be explained by demographic and genetic processes such as genetic swamping (Garrigan and Discussion Kingan, 2007) following the probable later migration of Neolithic populations, or neutral genetic drift (Serre and Pääbo, 2006), which After reviewing the evidence it is necessary to return to previ- could erase mitochondrial signals of low levels of introgression. If ous models of the speciation process. It would seem that the rela- Green et al.’s (2010) estimates of interbreeding are correct, they tionship between Neanderthals and AMH would best be would have to be considered biologically significant (Templeton, categorised as Mayr’s third stage of allopatry (Mayr et al., 1953): 2005), however the results have to be replicated with a much lar- occasional hybrids without free interbreeding, thus resulting in ger sample base. The disparity between genetic and morphological the conclusion that the two populations are each full species. This evidence could be allowed despite some hybridisation, as under a is the most conservative conclusion, given the sparse evidence for model of introgression of adaptive alleles from rare interbreeding hybrids in the archaeological record, with none of the supposed events, such alleles will probably be unrelated to morphology hybrids showing any necessary criteria except intermediate char- (Hawks et al., 2008). While genetic evidence fulfils some of the cri- acteristics, which are expected to appear long after the predicted teria for species identification, such as genotypic clusters which periods of interbreeding. The position is complicated further by would construe species status to both groups under the Genotypic the difficulty of identifying hybrids in the fossil record, as soft-tis- Cluster Species Concept (Mallet, 2007), it cannot prove genetic sue characteristics may be needed (Jolly, 2001). Nevertheless, even exclusivity as of yet. Nevertheless, the low estimates of interbreed- if hybridisation did occur, both groups maintained distinct mor- ing can be accepted under the original BSC. If we accept the genetic phological identities demonstrated by the lists of synapomorphies. Hybridisation did not lead to merging of these groups. This fact is primary evidence for arguing that they should be given species sta- tus under the Evolutionary Species Concept. No conclusive statement can be made on the existence of hybrids due to our limited knowledge of what a hybrid would look like, and the longevity of morphological indicators of hybridisation. The evidence itself is quite ambiguous (Klein, 2003), and could be explained by other processes such as homoplasy and convergent evolution. The clear separation of H. neanderthalensis and H. sapiens in the Levant could be taken to indicate cultural or biological sep- aration with minimal hybridisation, despite interaction in an area of contact (Kaufman, 2001). Regardless of the conclusion, the exis- tence of hybrids between populations has little bearing on their subsequent taxonomic assignment, as interbreeding can occur over many different levels, even between different genera (Jolly, 2001). To have relevance to the species debate, we would need accurate estimates of the level of interbreeding events towards the end of Fig. 2. Assumptions underlying use of genetics in taxonomic classification the Neanderthals evolutionary lifespan. Whereas Green et al. (Ferguson, 2002: 510). 44 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 evidence, including the contribution of supposed transitional hom- rion would result in a gross overestimation of the number of spe- inins in Africa and the Denisovan sister-group, we would have to cies, especially in plant taxonomy but also in mammals, as conclude that the speciation of H. sapiens was a long process with members of different genera and families regularly interbreed potentially frequent interbreeding events. without losing their cohesion as separate species. Considering The particular replacement pattern seen in Europe of AMH the time periods required for full speciation and the relatively spreading and eventually replacing the indigenous Neanderthal short lifespan of the Neanderthals, interbreeding should be population is of interest. Dobzhansky (1944) was the first to com- expected but is nonetheless irrelevant to their species status. ment that this pattern matched that of one species replacing the While genetic evidence seems to indicate some introgression of other. Neves and Serva (2011) came to a similar conclusion, how- Neanderthal and other hominin genes into the modern human ever with the more conservative statement that the extinction of genome, these results require wider replication, as well as further one subpopulation was expected under such long-term coexis- research into the ancestral genome before speciation occurred. tence. This would present a problem under the Ecological Species Morphological assessment provides little convincing evidence for Concept of Van Valen (1976), as such a pattern would only result the existence of hybrids, yet it may be more reliable to assume that from ecological competition and cohabitation of similar niches Neanderthals and AMH interbred, and thus that late Homo species (Garrigan and Kingan, 2007). This model could allow for some formed a syngameon. While molecular clocks have not progressed adaptive hybridisation, with the expanding population acquiring far enough to discover when introgression occurred relative to the advantageous genes from the indigenous population (Garrigan point of genetic divergence, it is clear that these two populations and Kingan, 2007), yet extinction by higher levels of hybridisation reached a sufficient stage of the speciation process that any inter- is impossible as the two groups did not merge into one taxon. breeding between them did not result in the merging of the taxa. Morphological analysis leads to a more certain conclusion. The The extinction of the Neanderthal lineage was not caused by existence of two separate morphospecies, with Neanderthals being hybridisation, with Neanderthals and AMH maintaining their more defined and easily differentiated by a list of traits, would ful- own evolutionary fate despite limited interbreeding. fil the requirements of the Phylogenetic Species Concept of Nixon The question has to be raised ‘‘Why is the species debate still so and Wheeler (1990), as well as traditional taxonomy and cladistics, prominent in the field of palaeoanthropology?’’. Gould’s (1991) where theoretically one autapomorphy is sufficient to define a spe- commentary on the races debate has some relevance here, as he cies (Simpson, 1951). It could also support species status under the has argued that such disputes do not further the study of variation Recognition Concept of Paterson (1981), as the large morphological between groups, and hinder the search for causal relationships differentiation would debatably have resulted in different species- between this variation and external influences. Considering this specific mate recognition systems (SMRS) (Tattersall and Schwartz, position, it could be argued that while the species debate remains 2006). The extinction of Neanderthals, potentially as late as 28 kya pertinent to issues of systematic classification and phylogenetics, (Finlayson et al., 2006; Hawks et al., 2008), would argue for sepa- its resolution will not contribute to our understanding of the bio- rate evolutionary fates, and thus support species status under the logical relationship between AMH and Neanderthals, as interbreed- Evolutionary Species Concept of Simpson (1951). ing cannot have had the significant effect required to alter Neanderthal species status. The only conclusion that can be Conclusion reached, regardless of further genetic evidence, is that Neanderthals and AMH constitute separate species in every meaning of the term. The aim of this synthesis was to assess the validity of the The knowledge that full biological speciation can occur in Homo in assumption that interbreeding between Neanderthals and AMH, the space of half a million years, despite significant periods of cul- as suggested by Green et al. (2010) among others, would require tural and geographic overlap between the groups, has wide impli- that the two be subsumed into H. sapiens. This assessment is cations. While some cultural behaviours may have permeated this dependent on proper understanding of the speciation process boundary, this did not prevent speciation from taking place. and methods of taxonomic classification. In this respect, it is clear that morphological and genetic evidence support the assignment of Neanderthals to a separate species, H. neanderthalensis. Evidence discussed regarding the main species concepts also confirms this Acknowledgments conclusion, with the two groups fulfilling all criteria. The only counterargument involves a recent misinterpretation of the Biolog- We would like to thank three anonymous Journal of Anthropo- ical Species Concept as requiring absolute genetic and reproductive logical Archaeology reviewers for their comments on earlier drafts isolation. This is understandable, but adherence to this strict crite- of the manuscript.

Appendix A. Appendix: Review of the eight main species concepts

Concept Proponent/s Definition Advantages Disadvantages Biological Mayr (1964), – ‘‘Species are groups of – Defines in terms of – Does not apply to asexual Dobzhansky (1935) interbreeding natural evolutionary causes of species organisms (Mayr, 1996)) populations that are (Ghiselin, 1974)) – Cannot be applied to fossil reproductively isolated from – Proposes a criterion for record (Tattersall, 1992; other such group’’ (Mayr, recognition (reproductive Boggs, 2001)) 1996: 264)Use morphological isolation) – Must be applied inferen- divergence as indication of tially through morphological degree of reproductive isola- analysis (Foley, 1991; Kimbel, tion (Mayr, 1996) 1991)) S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 45

Appendix A (continued) Concept Proponent/s Definition Advantages Disadvantages – Protected gene pool (Mayr – Cannot apply to allopatric and Ashlock, 1991)) populations (Tattersall, 1992; – Species are natural entities Quicke, 1993; Boggs, 2001)) (Balakrishnan, 2005)) – Based on assumptions of – Criterion: reproductive iso- evolutionary process, but ob- lation (Balakrishnan, 2005) serve pattern (Nixon and Wheeler, 1990)) – Ignores other evolutionary forces e.g. natural selection, ecologically mediated stabil- ising selection (Templeton, 1998; Mallet, 2007)) – True in principle, but un- testable (Mallet, 2007)) – Fails to recognise species in time (Kimbel, 1991; Balakrishnan, 2005) Cohesion Templeton (1989) – Cohesion through gene flow – Combines multiple – Does not distinguish (Mayr, 1996) concepts (Mallet, 2007) between internal and – Stresses ecological and external barriers to gene flow reproductive cohesion as (Mayr, 1996) maintaining species unity – Claims to be applicable to (Mallet, 2007) asexual taxa, when is not – Potential for phenotypic (Mayr, 1996) cohesion through intrinsic – Characterises evolutionary cohesion mechanisms lineage without indicating (Harrison, 1998) how to delineate (Mayr, 1996) – Does not explain how to deal with polytypic species (Mayr, 1996) Ecological Van Valen (1976) – ‘‘Lineage which occupies an – Does not apply to all cases adaptive zone minimally e.g. Cichlids (Mayr, 1996) different from that of any – Numerous cases of sympat- other lineage in its range and ric species occupying the which evolves separately same niche (Mayr, 1996) from all lineages outside its range’’ (Van Valen, 1976: 233) – Species maintained ecolog- ically, not reproductively (Van Valen, 1976) – Species are populations occupying different niches (Mayr, 1996) Evolutionary Simpson (1951), – ‘‘Phyletic lineage (ancestral- – Operational ‘recipe’ for – Undefined, vague terms Wiley (1978) descendent sequence of demarcation of fossil species (Mayr, 1996) interbreeding populations) (Mayr, 1996) – Only applicable to mono- evolving independently of – Acknowledges that species typic species (Mayr, 1996; others, with its own separate can maintain morphological Boggs, 2001) – and unitary evolutionary and ecological distinctness – No empirical criteria to test role and tendencies’’ despite genetic introgression (Mayr, 1996) (Simpson, 1951: 289) (Boggs, 2001) – Does not help in case of – ‘‘Ancestor-dependent pop- – Includes lineages effectively chronospecies (Mayr, 1996) ulations maintaining its separated from ancestral – Requires knowledge of identity from other lineages lineage that have not yet evolutionary history (Boggs, and which has its own evo- acquired reproductive isola- 2001) lutionary tendencies and tion (Miller, 2001) – Do not know historical fate fate’’ (Wiley, 1978: 18) – Acknowledges temporal of extant lineages (Quicke, – From recognition of inter- dimension of species (Mayr 1993) breeding between species and Ashlock, 1991) – Defines phyletic lineage, not (Boggs, 2001) species (Mayr and Ashlock,

(continued on next page) 46 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Appendix A (continued) Concept Proponent/s Definition Advantages Disadvantages 1991) Genotypic Mallet (1995, 2007) – ‘‘Separate species are – Practical application of the – Can be affected by (Mallet, cluster recognised if there are several Biological Species Concept 1995): clusters separated by (Mallet, 2007) – Sex-linked genes multilocus phenotypic or – Avoids tautological argu- – Chromosomal inversions genotypic gaps. A single ment (Mallet, 2007) – Polyploidy species ...is recognised if – Can identify majority of – Linkage disequilibrium there is only a single cluster genotypic clusters morpho- in the frequency distribution logically (Mallet, 2007) of multilocus phenotypes and – Includes polytypic species genotypes’’ (Mallet, 2007: 11) (Mallet, 1995) – Incorporates genetic and morphological indications of species (Mallet, 1995) Phenetic ‘‘Pheneticists’’(1960– – Defined in numerical or – Treats species as classes 70s) statistical terms (Mallet, – Similar to those already defined by traits of 2007) used by taxonomists (Mallet, organisms, not as individuals 2007) with properties necessary for – Practical and applicable to species category (Ghiselin, all cases (Balakrishnan, 2005) 1974) – Classifies by degree of resemblance, ignoring evolu- tionary theory (Ghiselin, 1974) Phylogenetic Cracraft (1983, – ‘‘The smallest diagnosable – Taxonomic units as units of – Ignores subspecies (multiple) 1987), Hennig cluster of individual evolution, therefore categories, so inapplicable to (1966); Nixon and organisms within which there applicable both to polytypic species (Tattersall, Wheeler (1990), is a parental pattern of evolutionary theory and 1992; Baum and Donoghue, Baum and Donoghue ancestry and descent’’ systematics (Tattersall, 1992; 1995) (1995) (Cracraft, 1983; 170) Kimbel, 1991) – Imprecise – different ap- – Revival of purely morpho- – Meets the requirements of proaches used to the defini- logical concept (Mayr, 1996) phylogenetic theory while tion of characters (Nixon and – Morphology taken to rep- avoiding dependence on pro- Wheeler, 1990) resent reproductive cohesive- cesses (Nixon and Wheeler, – Could overestimate number ness (Tattersall, 1992) 1990) of species (Quicke, 1993) – Species have fundamental – Acknowledges process of – Must reject character-based roles for systematics and speciation, and that infraspe- concepts as definitions ignore evolutionary theory cific taxa may be incipient evolutionary process (Baum (Tattersall, 1992) species (Nixon and Wheeler, and Donoghue, 1995) – Character-based (e.g. Nixon 1990) – Tautological: uses phylog- and Wheeler) and History/ – Integration of theoretical eny to determine species Lineage-based (e.g. Hennig, and operational viewpoints which are then used to esti- 1966; Baum and Donoghue, (Kimbel and Rak, 1993) mate the phylogeny (Mallet, 1995)(Balakrishnan, 2005) – Consistent with nature of 1995) species as individuals – Ignores Mendelian and (Kimbel, 1991) population genetics (Avise and Wollenberg, 1997) – Difficult to determine true fixation (Balakrishnan, 2005) Recognition Paterson (1981) – Species boundaries are – Acknowledges problems of – Same problems as found delimited by the shared Biological Species Concept with Biological Species specific-mate recognition and tries to incorporate Concept (Boggs, 2001) system (SMRS) (Paterson, solutions to these (Tattersall, – SMRS are generally exter- 1981) 1992) nal, and therefore hard to – Dependent on genealogical recognise in the fossil record role of species (Tattersall, (Tattersall, 1992) 1992) – Difficulty in application to – Most inclusive population humans and primates in gen- of individual, bi-parental eral, and therefore to the fos- organisms that share a com- sil record (Kimbel, 1991; Jolly, mon fertilisation system, 1993; Masters, 1993) S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 47

Appendix A (continued) Concept Proponent/s Definition Advantages Disadvantages represented by the SMRS – Can only diagnose species (Harrison, 1998) by tautology (Jolly, 1993) – May underestimate number of species (Kimbel, 1991)

References retrieval and analysis of five Neandertal mtDNA genomes. Science 325, 318– 321. Burrell, A.S., Jolly, C.J., Tosi, A.J., Disotell, T.R., 2009. Mitochondrial evidence for the Abi-Rached, L., Jobin, M.J., Kulkami, S., McWhinnie, A., Dalva, K., Gragert, L., hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Mol. Babrzadeh, F., Luo, M., Plummer, F.A., Kimani, J., Carrington, M., Middleton, D., Phylogenet. Evol. 51, 340–348. Rajalingam, R., Beksac, M., Marsh, S.G.E., Maiers, M., Guethlein, L.A., Tavoularis, Caramelli, D., Lalueza-Fox, C., Vernesi, C., Larl, M., Casoli, A., Mallegni, F., Chiarelli, B., S., Little, A.-M., Green, R.E., Norman, P.J., Parham, P., 2011. The shaping of Dupanloup, I., Bertranpetit, J., Barbujani, G., Bertorelle, G., 2003. Evidence for a modern human immune systems by multiregional admixture with archaic genetic discontinuity between Neandertals and 24,000-year-old anatomically humans. Science 334, 89–94. modern Europeans. Proc. Natl. Acad. Sci. 100, 6593–6597. Ackermann, R.R., 2010. Phenotypic traits of primate hybrids: recognizing admixture Caramelli, D., Lalueza-Fox, C., Condemi, S., Longo, L., Milani, L., Manfredini, A., de in the fossil record. Evol. Anthropol. 19 (6), 258–270. Saint Pierre, M., Adoni, F., Lari, M., Giunti, P., Ricci, S., Casoli, A., Calafell, F., Ackermann, R.R., Bishop, J.M., 2009. Morphological and molecular evidence reveals Mallegni, F., Bertranpetit, J., Stanyon, R., Bertorelle, G., Barbujani, G., 2006. A recent hybridization between taxa. Evolution 64, 271–290. highly divergent mtDNA sequence in a Neandertal individual from Italy. Curr. Ahern, J.C.M., 2006. Non-metric variation in recent humans as a model for Biol. 16, R630–R632. understanding Neanderthal- differences: just how Churchill, S.E., Smith, F.H., 2000. A modern human humerus from the early ‘‘unique’’ are Neanderthal unique traits? In: Harvati, K., Harrison, T. (Eds.), Aurignacian of Vogelherdhöhle (Stetten, Germany). Am. J. Phys. Anthropol. 112, Neanderthals Revisited: New Approaches and Perspectives. Springer, Dordrecht, 251–273. pp. 255–268. Cortés-Ortiz, L., Duda Jr., T.F., Canales-Espinosa, D., García-Orduña, F., Rodríguez- Ahern, J.C.M., Lee, S.-H., Hawks, J.D., 2002. The late Neandertal supraorbital fossils Luna, E., Bermingham, E., 2007. Hybridization in large-bodied new world from Vindija Cave, Croatia: a biased sample? J. Hum. Evol. 43, 419–432. primates. Genetics 176, 2421–2425. Alves, I., Hanulová, A.Š., Foll, M., Excoffier, L., 2012. Genomic data reveal a complex Cracraft, J., 1983. Species concepts and species analysis. Curr. Ornithol. 1, 159–187. making of humans. PLoS Genet. 8, e1002837. Currat, M., Excoffier, L., 2004. Modern humans did not admix with Neanderthals Arnold, M.L., Meyer, A., 2006. Natural hybridization in primates: One evolutionary during their range expansion into Europe. PLoS Biol. 2, 2264–2274. mechanism. Zoo. 109, 261–276. Currat, M., Excoffier, L., 2011. Strong reproductive isolation between humans and Arnold, M.L., Meyer, A., 2006. Natural hybridization in primates: one evolutionary Neanderthals inferred from observed patters of introgression. Proc. Natl. Acad. mechanism. Zoology 109, 261–276. Sci. 108, 15129–15134. Arthreya, S., 2009. A comparative study of frontal bone morphology among Dabney, J., Knapp, M., Glocke, I., Gansauge, M.-T., Weihmann, A., Nickel, B., Pleistocene hominin fossil groups. J. Hum. Evol. 57, 786–804. Valdiosera, C., Garcia, N., Pääbo, S., Arsuaga, J.-L., Meyer, M., 2013. Proc. Natl. Avise, J.C., Wollenberg, K., 1997. Phylogenetics and the origin of species. Proc. Natl. Acad. Sci. 110, 15758–15763. Acad. Sci. 94, 7748–7755. Dalén, L., Orlando, L., Shapiro, B., Durling, M.B., Quam, R., Gilbert, M.T.P., Fernández- Bailey, S.E., 2002. A closer look at Neanderthal postcanine dental morphology: the Lomana, J.C.D., Willerslev, E., Arsuaga, J.L., Götherstrom, A., 2012. Partial genetic mandibular dentition. Anat. Rec. 269, 148–156. turnover in neandertals: continuity in the east and population replacement in Bailey, S.E., Lynch, J.M., 2005. Diagnostic differences in mandibular P4 shape the west. Mol. Biol. Evol. 29, 1893–1897. between Neandertals and anatomically modern humans. Am. J. Phys. Anthropol. de Queiroz, K., 1998. The general lineage concept of species, species criteria, and the 126, 268–277. process of speciation: a conceptual unification and terminological Balakrishnan, R., 2005. Species concepts, species boundaries and species recommendations. In: Howard, D.J., Berloche, S.H. (Eds.), Endless Forms: identification: a view from the tropics. Syst. Biol. 54, 689–693. Species and Speciation. Oxford University Press, New York, pp. 57–75. Barton, N.H., 2006. Evolutionary biology: how did the human species form? Curr. de Queiroz, K., 2005. Different species problems and their resolution. BioEssays 27, Biol. 16, R647–R650. 1263–1269. Barton, C.M., Riel-Salvatore, J., 2012. Agents of change: modeling biocultural de Vos, J., 2009. Receiving an ancestor into the phylogenetic tree: Neanderthal man, evolution in upper pleistocene western Eurasia. Adv. Compl. Syst. 15, 1150003- Homo erectus and Homo floresiensis: L’histoire se repete. J. Hist. Biol. 42, 361– 1–1150003-24. 379. Baum, D.A., Donoghue, M.J., 1995. Choosing among alternative ‘‘phylogenetic’’ Delson, E., Tattersall, I., Van Couvering, J.A. (Eds.), 2000. Encyclopedia of Human species concepts. Syst. Bot. 20, 560–573. Evolution and , second ed. Garland Publishing Inc., New York. Bayle, P., Macchiarelli, R., Trinkaus, E., Duarte, C., Mazurier, A., Zilhão, J., 2010. Di Vincenzo, F., Churchill, S.E., Manzi, G., 2012. The Vindija Neanderthal scapular Dental maturational sequence and dental tissue proportions in the early Upper glenoid fossa: comparative shape analysis suggests evo-devo changes among child from Abrigo do Lagar Velho, Portugal. Proc. Natl. Acad. Sci. 107, Neanderthals. J. Hum. Evol. 62, 274–285. 1338–1342. Dobzhansky, T., 1935. A critique of the species concept in biology. Philos. Sci. 2, Beauval, C., Maureille, B., Lacrampe-Cuyaubere, F., Serre, D., Peressinotto, D., Bordes, 344–355. J.G., Cochard, D., Couchoud, I., Dubrasquet, D., Laroulandie, V., Lenoble, A., Dobzhansky, T., 1944. On species and races of living and fossil man. Am. J. Phys. Mallye, J.-B., Pasty, S., Primault, J., Rohland, N., Pääbo, S., Trinkaus, E., 2005. A Anthropol. 2, 251–265. late Neandertal femur from Les Rochers-de-Villeneuve, France. Proc. Natl. Acad. Duarte, C., Mauricio, J., Pettitt, P.B., Souto, P., Trinkaus, E., 1999. The early Sci. 102, 7085–7090. Upper Paleolithic human skeleton from the Abrigo do Lagar Velho (Portugal) Beerli, P., Edwards, S.V., 2002. When did Neanderthals and modern humans and modern human emergence in Iberia. Proc. Natl. Acad. Sci. 96, diverge? Evol. Anthropol. 11, 60–63. 7604–7609. Belle, E.M.S., Benazzo, A., Ghirotto, S., Colonna, V., Barbujani, G., 2009. Comparing Durand, E.Y., Patterson, N., Reich, D., Slatkin, M., 2011. Testing for ancient admixture models on the genealogical relationships among Neandertal, Cro-Magnoid and between closely related populations. Mol. Biol. Evol. 28, 2239–2252. modern Europeans by serial coalescent simulations. Heredity 102, 218–225. Endicott, P., Ho, S.Y.W., 2008. A Bayesian evaluation of human mitochondrial Boggs, C.L., 2001. Species and speciation. In: Smelser, N., Baltes, P. (Eds.), substitution rates. Am. J. Hum. Genet. 82, 895–902. International Encyclopedia of the Social and Behavioral Sciences. Elsevier, Endicott, P., Ho, S.Y.W., Stringer, C., 2010. Using genetic evidence to evaluate four Oxford, pp. 14855–14861. palaeoanthropological hypotheses for the timing of Neanderthal and modern Bower, B., 2006. Hybrid-driven evolution. Science 169, 308–309. human origins. J. Hum. Evol. 59, 87–95. Bräuer, G., Broeg, H., Stringer, C.B., 2006. Earliest Upper Paleolithic crania from Eriksson, A., Manica, A., 2012. Effect of ancient population structure on the degree of Mladecˇ, Czech Republic, and the question of Neanderthal-modern continuity: polymorphism shared between modern human populations and ancient metrical evidence from the fronto-facial region. In: Harvati, K., Harrison, T. hominins. Proc. Natl. Acad. Sci. 35, 13956–13960. (Eds.), Neanderthals Revisited: New Approaches and Perspectives. Springer, Ferguson, J.W.H., 2002. On the use of genetic divergence for identifying species. Biol. Dordrecht, pp. 269–290. J. Linn. Soc. Lond. 75, 509–516. Briggs, A.W., Good, J.M., Green, R.E., Krause, J., Maricic, T., Stenzel, U., Lalueza-Fox, C., Finlayson, C., Pacheco, F.G., Rodríguez-Vidal, J., Fa, D.A., Gutierrez López, J.M., Rudan, P., Brajkovic, D., Kucan, Z., Gusic, I., Schmitz, R., Doronichev, V.B., Santiago Pérez, A., Finlayson, G., Allue, E., Baena Preysler, J., Cáceres, I., Carrión, Golovanova, L.V., de la Rasilla, M., Fortea, J., Rosas, A., Pääbo, S., 2009. Targeted J.S., Fernández Jalvo, Y., Gleed-Owen, C.P., Jimenez Espejo, F.J., López, P., López 48 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Sáez, J.A., Riquelme Cantal, J.A., Sánchez Marco, A., Guzman, F.G., Brown, K., Hey, J., Waples, R.S., Arnold, M.L., Butlin, R.K., Harrison, R.G., 2003. Understanding Fuentes, N., Valarino, C.A., Villalpando, A., Stringer, C.B., Martinez Ruiz, F., and confronting species uncertainty in biology and conservation. Trends Ecol. Sakamoto, T., 2006. Late survival of Neanderthals at the southernmost extreme Evol. 18, 597–603. of Europe. Nature 443, 850–853. Higham, T., Ramsey, C.B., Karavanic´, I., Smith, F.H., Trinkaus, E., 2006. Revised direct

Fitzpatrick, B.M., 2004. Rates of evolution of hybrid inviability in birds and radiocarbon dating of the Vindija G1 Upper Paleolithic Neandertals. Proc. Natl. mammals. Evolution 58, 1865–1870. Acad. Sci. 103, 553–557. Foley, R.A., 1991. How many species of hominid should there be? J. Hum. Evol. 20, Holliday, T.W., 2003. Species concepts, reticulation, and . Curr. 413–427. Anthropol., 653–660. Forhan, G., Martiel, J.-L., Blum, M.G.B., 2008. A deterministic model of admixture Holliday, T.W., 2006. Neanderthals and modern humans: an example of a and genetic introgression: the case of Neanderthal and Cro-Magnon. Math. mammalian syngameon? In: Harvati, K., Harrison, T. (Eds.), Neanderthals Biosci. 216, 71–76. Revisited: New Approaches and Perspectives. Springer, Dordrecht, pp. 281–298. Frayer, D.W., Jelínek, J., Oliva, M., Wolpoff, M.H., 2006. Aurignacian male crania, Holmes, E.C., Pesole, G., Saccone, C., 1989. Stochastic models of molecular evolution jaws and teeth from the Mladecˇ Caves, Moravia, Czech Republic. In: Tescheler- and the estimation of phylogeny and rates of nucleotide substitution in the Nicola, M. (Ed.), Early Modern Humans at the Moravian Gate: The Mladecˇ Caves hominoid primates. J. Hum. Evol. 18, 775–794. and Their Remains. Springer, Vienna, pp. 185–272. Huxley, T.H., 1863. Evidence as to Man’s Place in Nature. Williams and Norgate, Fu, Q., Mittnik, A., Johnson, P.L.F., Bos, K., Lari, M., Bollongino, R., Sun, C., Giemsch, L., London. Schmitz, R., Burger, J., Ronchitelli, A.M., Martini, F., Cremonesi, R.G., Svoboda, S., Jensen-Seaman, M.I., Hooper-Boyd, K.A., 2008. Molecular clocks: Determining the Reich, D., Pääbo, S., Krause, J., 2013. A revised timescale for human evolution age of the human–chimp divergence. In: Encyclopedia of Life Sciences (ELS). based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559. John Wiley & Sons, Ltd., http://dx.doi.org/10.1002/ Garrigan, D., Kingan, S.B., 2007. Archaic human admixture: a view from the genome. 9780470015902.a0020813. Curr. Anthropol. 48, 895–902. Jolly, C.J., 1993. Species, subspecies, and baboon systematic. In: Kimbel, W.H., Garrigan, D., Mobasher, Z., Kingan, S.B., Wilder, J.A., Hammer, M.F., 2005. Deep Martin, L.B. (Eds.), Species, Species Concepts, and Primate Evolution. Plenum haplotype divergence and long-range linkage disequilibrium at Xp21.1 provide Press, New York, pp. 67–101. evidence that humans descend from a structured ancestral population. Genetics Jolly, C.J., 2001. A proper study for mankind: analogies from the papionin monkeys 170, 1849–1856. and their implications for human evolution. Yearbook Phys. Anthropol. 44, 177– Ghirotto, S., Tassi, F., Benazzo, A., Barbujani, G., 2011. No evidence of Neandertal 204. admixture in the mitochondrial genomes of early European modern humans Kaufman, D., 2001. Comparisons and the case for interaction among Neanderthals and contemporary Europeans. Am. J. Phys. Anthropol. 146, 242–252. and early modern humans in the levant. Oxf. J. Archaeol. 20, 219–240. Ghiselin, M.T., 1974. A radical solution to the species problem. Syst. Zool. 23, 536– Keita, S.O.Y., Kittles, R.A., Royal, C.D.M., Bonney, G.E., Furbert-Harris, P., Dunston, 544. G.M., Rotimi, C.N., 2004. Conceptualising human variation. Nat. Genet. 36, S17– Giles, R.E., Blanc, H., Cann, H.M., Wallace, D.C., 1980. Maternal inheritance of human S20. mitochondrial DNA. Proc. Natl. Acad. Sci. 77, 6715–6719. Kimbel, W.H., 1991. Species, species concepts and hominid evolution. J. Hum. Evol. Gould, S.J., 1991. Why we should not name human races – a biological view. In: 20, 355–371. Gould, S.J. (Ed.), Ever Since Darwin: Reflections in Natural History. Penguin Kimbel, W.H., Rak, Y., 1993. The importance of species taxa in Books, St. Ives, pp. 231–237. and an argument for the phylogenetic species concept. In: Kimbel, W.H., Martin, Grant, B.R., Grant, P.R., 1998. Hybridization and speciation in Darwin’s finches. In: L.B. (Eds.), Species, Species Concepts and Primate Evolution. Plenum Press, New Howard, D.J., Berloche, S.H. (Eds.), Endless Forms: Species and Speciation. York, pp. 461–484. Oxford University Press, New York, pp. 404–422. King, W., 1984. The reputed fossil man of the Neanderthal. Q. Rev. Sci. 1, 88–97. Green, R.E., Krause, J., Ptak, S.E., Briggs, A.W., Ronan, M.T., Simons, J.F., Du, L., Klein, R.G., 2003. Whither the Neanderthals? Science 299, 1525–1527. Egholm, M., Rothberg, J.M., Paunovic, M., Pääbo, S., 2006. Analysis of one million Klein, R.G., 2008. Out of Africa and the evolution of human behavior. Evol. base pairs of Neanderthal DNA. Nature 444, 330–336. Anthropol. 17, 267–281. Green, R.E., Malaspinas, A.-S., Krause, J., Briggs, A.W., Johnson, P.L.F., Uhler, C., Knight, A., 2003. The phylogenetic relationship of Neandertal and modern human Meyer, M., Good, J.M., Maricic, T., Stenzel, U., Prufer, K., Siebauer, M., Burbano, mitochondrial based on informative nucleotide sites. J. Hum. Evol. 44, H.A., Ronan, M., Rothberg, J.M., Egholm, M., Rudan, P., Brajkovic, D., Kucan, Z., 627–632. Gusic, I., Wikstrom, M., Laakkonen, L., Kelso, J., Slatkin, M., Pääbo, S., 2008. A Krause, J., Fu, Q., Good, J.M., Viola, B., Shunkov, M.V., Derevianko, A.P., Pääbo, S., complete Neandertal mitochondrial genome sequence determined by high- 2010. The complete mitochondrial DNA genome of an unknown hominin from throughput sequencing. Cell 134, 416–426. southern Siberia. Nature 464, 894–897. Green, R.E., Briggs, A.W., Krause, J., Prufer, K., Lachmann, M., Pääbo, S., 2009. The Krings, M., Geisert, H., Schmitz, R.W., Krainitzki, H., Pääbo, S., 1999. DNA sequence Neandertal genome and ancient DNA authenticity. EMBO J. 28, 2494–2502. of the mitochondrial hypervariable region II from the Neandertal type Green, R.E., Krause, J., Briggs, A.W., Maricic, T., Stenzel, U., Kircher, M., Patterson, N., specimen. Proc. Natl. Acad. Sci. 96, 5581–5585. Li, H., Zhai, W., Fritz, M.H.-Y., Hansen, N.F., Durand, E.Y., Malaspinas, A.-S., Krings, M., Capelli, C., Tschentscher, F., Geisert, H., Meyer, S., von Haeseler, A., Jensen, J.D., Marques-Bonet, T., Alkan, C., Prüfer, K., Meyer, M., Burbano, H.A., Grossschmidt, K., Possnert, G., Paunovic, M., Pääbo, S., 2000. A view of Good, J.M., Schultz, R., Aximu-Petri, A., Butthof, A., Höffner, B., Siegemund, M., Neandertal genetic diversity. Nat. Genet. 26, 144–146. Weihmann, A., Nusbaum, C., Lander, E.S., Russ, C., Novod, N., Affourtit, J., Krings, M., Stone, A., Schmitz, R.W., Krainitzki, H., Stoneking, M., Pääbo, S., 2006. Egholm, M., Verna, C., Rudan, P., Brajkovic, D., Kucan, Zˇ., Gušic, I., Doronichev, Neandertal DNA sequences and the origin of modern humans. In: Ciochon, R.L., V.B., Golovanova, L.V., Lalueza-Fox, C., de la Rasilla, M., Fortea, J., Rosas, A., Fleagle, J.G. (Eds.), The Human Evolution Source Book. Pearson Prentice Hall, Mullikin, J.C., Slatkin, M., Nielsen, R., Kelso, J., Lachmann, M., Reich, D., Pääbo, S., Upper Saddle River, NJ, pp. 471–480. 2010. A draft sequence of the Neandertal genome. Science 328, 710–722. Kupczik, K., Hublin, J.-J., 2010. Mandibular molar root morphology in Neanderthals Hammer, M.F., Woerner, A., Mendez, F.L., Watkins, J.C., Wall, J.D., 2011. Genetic and Late Pleistocene and recent Homo sapiens. J. Hum. Evol. 59, 525–541. evidence for archaic admixture in Africa. Proc. Natl. Acad. Sci. 108, 15123– Lalueza-Fox, C., Sampietro, M.L., Caramelli, D., Puder, Y., Lari, M., Calafell, F., 15128. Martinez-Maza, C., Bastir, M., Fortea, J., de la Rasilla, M., Nertranpetot, J., Rosas, Harrison, R.G., 1998. Linking evolutionary patter and process: the relevance of A., 2005. Neandertal evolutionary genetics; mitochondrial DNA data from the species concepts for the study of speciation. In: Howard, D.J., Berloche, S.H. . Mol. Biol. Evol. 22, 1077–1081. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, New Lalueza-Fox, C., Krause, J., Caramelli, D., Catalano, G., Milani, L., Sampietro, L., York, pp. 19–31. Calafell, F., Martínez-Maza, C., Bastir, M., García-Tabernero, A., De la Rasilla, M., Harvati, K., 2003. The Neanderthal taxonomic position: models of intra- and inter- Fortea, J., Pääbo, S., Bertranpetit, J., Rosas, A., 2006. Mitochondrial DNA of an specific craniofacial variation. J. Hum. Evol. 44, 107–132. Iberian Neandertal suggests a population affinity with other European Harvati, K., Frost, S.R., McNulty, K.P., 2004. Neanderthal taxonomy reconsidered: Neandertals. Curr. Biol. 16, R629–R630. implications of 3D primate models of intra- and interspecific differences. Proc. Lalueza-Fox, C., Rosas, A., de la Rasilla, M., 2012. Issues from Neandertal genomics: Natl. Acad. Sci. 101, 1147–1152. diversity, adaptation and hybridisation revised from the El Sidrón case study. Harvati, K., Gunz, P., Grigorescu, D., 2007. Cioclovina (Romania): affinities of an Quatern. Int. 247, 10–14. early modern European. J. Hum. Evol. 53, 732–746. Langergraber, K.E., Prüfer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., Inoue, Hawks, J., 2006. Selection on mitochondrial DNA and the Neanderthal problem. In: E., Inoue-Muruyama, M., Mitani, J.C., Muller, M.N., Robbins, M.M., Schubery, G., Harvati, K., Harrison, T. (Eds.), Neanderthals Revisited: New Approaches and Stoinski, T.S., Viola, B., Watts, D., Wittig, R.M., Wrangham, R.C., Zuberbühler, K., Perspectives. Springer, Dordrecht, pp. 221–238. Pääbo, S., Vigilant, L., 2013. Generation times in wild chimpanzees and gorillas Hawks, J.D., Wolpoff, M.H., 2006. The accretion model of Neandertal evolution. In: suggest earlier divergence times in great and human evolution. Proc. Natl. Ciochon, R.L., Fleagle, J.G. (Eds.), The Human Evolution Source Book. Pearson Acad. Sci. 109 (39), 15716–15721. Prentice Hall, Upper Saddle River, NJ, pp. 458–470. Lindahl, T., 1997. Facts and artifacts of ancient DNA. Cell 90, 1–3. Hawks, J., Cochran, G., Harpending, H.C., Lahn, B.T., 2008. A genetic legacy from Linnaeus, C., 1802. A General System of Nature: Through the Three Kingdoms of archaic Homo. Trends Genet. 24, 19–23. Animals, Vegetables and Minerals. Lackington, Allen and Co., London. Hennig, W., 1966. Phylogenetic Systematics. University of Illinois Press, Urbana. Livingstone, F.B., Dobzhansky, T., 1962. On the non-existence of human races. Curr. Hershkovitz, I., Smith, P., Sarig, R., Quam, R., Rodríguez, L., García, R., Arsuaga, J.L., Anthropol. 3, 279–281. Barkai, R., Gopher, A., 2011. Middle Pleistocene dental remains from Qesem Lohse, K., Frantz, L.A.F., 2013. Maximum Likelihood Evidence for Neandertal Cave (Israel). Am. J. Phys. Anthropol. 144, 575–592. Admixture in Eurasian Populations from Three Genomes. arXiv preprint Hey, J., 2006. On the failure of modern species concepts. Trends Ecol. Evol. 21, 447– arXiv: 1307.8263. 450. S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 49

Long, J.C., Kittles, R.A., 2003. Human genetic diversity and the nonexistence of Reich, D., Green, R.E., Kircher, M., Krause, J., Patterson, N., Durand, E.Y., Viola, B., biological races. Hum. Biol. 75, 449–471. Briggs, A.W., Stenzel, U., Johnsonm, P.L.F., Maricic, T., Good, J.M., Marques-Bonet, Loogväli, E.-L., Kivisild, T., Margus, T., Villems, R., 2009. Explaining the imperfection T., Alkan, C., Fu, Q., Mallick, S., Li, H., Meyer, M., Eichler, E.E., Stoneking, M., of the molecular clock of hominid mitochondria. PLoS ONE 4, e8260. Richards, M., Talamo, S., Shunkov, M.V., Derevianko, A.P., Hublin, J.-J., Kelos, J., Lotsy, J.P., 1925. Species or Linneon? Genetica 7 (5–6), 475–486. Slatkin, M., Pääbo, S., 2010. Genetic history of an archaic hominin group from Lowery, R.K., Uribe, G., Jimenez, E.B., Weiss, M.A., Herrera, K.J., Regueiro, M., Herrera, Denisova Cave in Siberia. Nature 468, 1053–1060. R.J., 2013. Neanderthal and Denisova genetic affinities with contemporary Reydon, T.A.C., 2004. Why does the species problem still persist? BioEssays 26, 300– humans: introgression versus common ancestral polymorphisms. Gene 530, 305. 83–94. Rougier, H., Milota, Sß., Rodrigo, R., Gherase, M., Sarcina˘, Moldovan, O., Zilhão, J., Mallet, J., 1995. A species definition for the modern synthesis. Tree 10, 294–299. Constantin, S., Franciscus, R.G., Zollikofer, C.P.E., Ponce de León, M., Trinkaus, E., Mallet, J., 2007. Concepts of species. In: Levin, S.A. (Ed.), Encyclopedia of 2007. Pesßtera cu Oase 2 and the cranial morphology of early modern Europeans. Biodiversity. Academic Press, New York, pp. 427–440. Proc. Natl. Acad. Sci. 104, 1165–1170. Masters, J.C., 1993. Primates and paradigms: problems with the identification of Sánchez-Quinto, F., Botigué, L.R., Civit, S., Arenas, C., Ávila-Arcos, M., Bustamente, genetic species. In: Kimbel, W.H., Martin, L.B. (Eds.), Species, Species Concepts, C.D., Comas, D., Lalueza-Fox, C., 2012. North African populations carry the and Primate Evolution. Plenum Press, New York, pp. 43–64. signature of admixture with Neandertals. PLoS ONE 7, e47765. Max Planck Institute for Evolutionary Anthropology, 2013. A High-quality Sankararaman, S., Patterson, N., Li, H., Pääbo, S., Reich, D., 2012. The date of Neandertal Genome Sequence. (accessed 03.10.13). e1002947. Mayr, E., 1964. Systematics and the Origin of Species: From the Viewpoint of a Santa Luca, A.P., 1978. A re-examination of presumed Neandertal-like fossils. J. Zoologist. Dover Publications Inc., UK. Hum. Evol. 7, 619–636. Mayr, E., 1996. What is a species, and what is not? Philos. Sci. 63, 262–277. Schmitz, R.W., Serre, D., Bonani, G., Fein, S., Hillgruber, F., Krainitzki, H., Pääbo, S., Mayr, E., Ashlock, P.D., 1991. Principles of Systematic Zoology, second ed. McGraw- Smith, F.H., 2002. The Neandertal type site revisited: interdisciplinary Hill, New York. investigations of skeletal remains from the Neander Valley, Germany. Proc. Mayr, E., Gorton Linsley, E., Usinger, R.L., 1953. Methods and Principles of Natl. Acad. Sci. 99, 13342–13347. Systematic Zoology. McGraw-Hill Book Company Inc., New York. Scholz, M., Bachmann, L., Nicholson, G.J., Bachmann, J., Giddings, I., Ruschoff-Thale, Mendez, F.L., Watkins, J.C., Hammer, M.E., 2012. A haplotype at STAT2 introgressed B., Czarnetzki, A., Pusch, C.M., 2000. Genomic differentiation of neanderthals from Neanderthals and serves as a candidate of positive selection in Papua New and anatomically modern man allows a fossil-DNA-based classification of Guinea. Am. J. Hum. Genet. 91, 265–274. morphologically indistinguishable hominid bones. Am. J. Hum. Gen. 66, 1927– Meyer, M., Kircher, M., Gansuage, M.-T., Li, H., Racimo, F., Mallick, S., Schraiber, J.G., 1932. Jay, F., Prüfer, K., de Filippo, C., Sudmant, P.H., Alkan, C., Fu, Q., Do, R., Rohland, Schwartz, J.H., Tattersall, I., 1996. Significance of some previously unrecognized N., Tandon, A., Siebauer, M., Green, R.E., Bryc, K., Briggs, A.W., Stenzel, U., apomorphies in the nasal region of Homo neanderthalensis. Proc. Natl. Acad. Sci. Dabney, J., Shendure, J., Kitzman, J., Hammer, M.F., Shunkov, M.V., Derevianko, 93, 10854–10952. A., Patterson, N., Andrés, A.M., Eichler, E.E., Slatkin, M., Reich, D., Kelso, J., Pääbo, Serre, D., Pääbo, S., 2006. The fate of European Neanderthals: results and S., 2012. A high-coverage sequence from an archaic denisovan individual. perspectives from ancient DNA analyses. In: Harvati, K., Harrison, T. (Eds.), Science 338, 222–226. Neanderthals Revisited: New Approaches and Perspectives. Springer, Dordrecht, Miller III, W., 2001. The structure of species, outcomes of speciation and the ‘species pp. 211–220. problem’: ideas for paleobiology. Palaeogeogr. Palaeoclimatol. Palaeoecol. 176, Serre, D., Langaney, A., Chech, M., Teschler-Nicola, M., Paunovic, M., Mennecier, P., 1–10. Hofrieter, M., Possnert, G., Pääbo, S., 2004. No evidence of Neandertal mtDNA Minugh-Purvis, N., Viola, T.B., Teschler-Nicola, M., 2006. The Mladecˇ 3 infant. In: contribution to early modern humans. PLoS Biol. 2, 0313–0317. Tescheler-Nicola, M. (Ed.), Early Modern Humans at the Moravian Gate: The Shaw, K.L., 1998. Species and the diversity of natural groups. In: Howard, D.J., Mladecˇ Caves and Their Remains. Springer, Vienna, pp. 357–383. Berloche, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Neves, A.G.M., Serva, M., 2011. Extremely Rare Interbreeding Events can Explain Press, New York, pp. 44–56. Neanderthal DNA in Modern Humans. arXiv:1103.4621v2. Simpson, G.G., 1943. Criteria for genera, species, and subspecies in zoology and Nixon, K.C., Wheeler, Q.D., 1990. An amplification of the phylogenetic species paleozoology. Ann. N. Y. Acad. Sci. 44, 145–178. concept. Cladistics 6, 211–223. Simpson, G.G., 1951. The species concept. Evolution 5, 285–298. Noonan, J.P., Coop, G., Kudaravalli, S., Smith, D., Krause, J., Alessi, J., Chen, F., Platt, D., Simpson, G.G., 1961. Principles of Taxonomy. Columbia University Press, Pääbo, S., Pritchard, J.K., Rubin, E.M., 2006. Sequencing and analysis of New York. Neanderthal genomic DNA. Science 314, 1113–1118. Sites, J.W., Marshall, J.C., 2004. Operational criteria for delimiting species. Annu. Nordberg, M., 1998. On the probability of Neanderthal ancestry. Am. J. Hum. Genet. Rev. Ecol. Evol. Syst. 35, 199–227. 63, 1237–1240. Smith, A.B., 1994. Systematics and the Fossil Record: Documenting Evolutionary Orlando, L., Darlu, P., Toussaint, M., Bonjean, D., Otte, M., Hanni, C., 2006. Revisiting Patterns. Blackwell Scientific, Oxford. Neandertal diversity with a 100,000 year old mtDNA sequence. Curr. Biol. 16, Soficaru, A., Dobos, A., Trinkaus, E., 2006. Early modern humans from the Pesßtera R400–R402. Muierii, Baia de Fier, Romania. Proc. Natl. Acad. Sci. 103, 17196–17201. O’Rourke, D.H., Hayes, M.G., Carlyle, S.W., 2000. Ancient DNA studies in physical Soficaru, A., Petrea, C., Dobosß, A., Trinkaus, E., 2007. The human cranium from the anthropology. Annu. Rev. Anthropol. 29, 217–242. Pesßtera Cioclovina Uscata˘, Romania: context, age, taphonomy, morphology and Ovchinnikov, I.V., Gotherstroms, A., Romanova, G.P., Kharitonov, V.M., Liden, K., paleopathology. Curr. Anthropol. 48, 611–619. Goodwin, W., 2000. Molecular analysis of Neanderthal DNA from the northern Spoor, F., Hublin, J.-J., Braun, M., Zonneveld, F., 2003. The bony labyrinth of Caucasus. Nature 404, 490–493. Neanderthals. J. Hum. Evol. 44, 141–165. Pääbo, S., 2003. The mosaic that is our genome. Nature 421, 409–412. Stringer, C., 2012. The Origins of Our Species. Penguin Group, England. Paterson, H.E.H., 1981. The continuing search for the unknown and unknowable: a Stringer, C.B., Andrews, P., 1988. Genetic and fossil evidence for the origin of critique of contemporary ideas on speciation. S. Afr. J. Sci. 77, 113–119. modern humans. Science 239, 1263–1268. Patterson, N., Richter, D.J., Gnerre, S., Lander, E.S., Reich, D., 2006. Genetic evidence Tattersall, I., 1986. Species recognition in human . J. Hum. Evol. 15, for complex speciation of humans and chimpanzees. Nature 44, 1103–1108. 165–175. Pettitt, P., 2011. The Palaeolithic Origins of Human Burial. Routledge, London. Tattersall, I., 1992. Species concepts and species identification in human evolution. Prufer, K., Racimo, F., Patterson, N., Jay, F., Sankararaman, S., Sawyer, S., Heinze, A., J. Hum. Evol. 22, 341–349. Renaud, G., Sudmant, P.H., de Filippo, C., Li, H., Mallick, S., Dannemann, M., Fu, Tattersall, I., 1993. Speciation and morphological differentiation in the genus Lemur. Q., Kircher, M., Kuhlwilm, M., Lachmann, M., Meyer, M., Ongyerth, M., Siebauer, In: Kimbel, W., Martin, L. (Eds.), Species, Species Concepts, and Primate M., Theunert, C., Tandon, A., Moorjani, P., Pickrell, J., Mullikin, J.C., Vohr, S.H., Evolution. Wiley, New York, pp. 163–176. Green, R.E., Hellmann, I., Johnson, P.L.F., Blanche, H., Cann, H., Kitzman, J.O., Tattersall, I., 2007. Neanderthals, Homo sapiens, and the question of species in Shendure, J., Eichler, E.E., Lein, E.S., Bakken, T.E., Golovanova, L.V., Doronichev, paleoanthropology. J. Anthropol. Sci. 85, 139–146. V.B., Shunkov, M.V., Derevianko, A.P., Viola, B., Slatkin, M., Reich, D., Kelso, J., Tattersall, I., Schwartz, J.H., 1998. Morphology, paleoanthropology, and Paabo, S., 2014. The complete genome sequence of a Neanderthal from the Altai Neanderthals. Anatom. Rec. 253, 113–117. Mountains. Nature 505, 43–49. Tattersall, I., Schwartz, J.H., 1999. Hominids and hybrids: the place of Neanderthals Pulquério, M.J.F., Nichols, R.A., 2007. Dates from the molecular clock: how wrong in human evolution. Proc. Natl. Acad. Sci. 96, 7117–7119. can we be? Trends Ecol. Evol. 22, 180–184. Tattersall, I., Schwartz, J.H., 2006. The distinctiveness and systematic context of Quicke, D.L.J., 1993. Principles and Techniques of Contemporary Taxonomy. Blackie Homo neanderthalensis. In: Harvati, K., Harrison, T. (Eds.), Neanderthals Academic & Professional, Tertiary Level Biology, Glasgow. Revisited: New Approaches and Perspectives. Springer, Dordrecht, pp. 9–22. Quintyn, C., 2009. The naming of new species in hominin evolution: a radical Templeton, A.R., 1989. The meaning of species and speciation: A genetic proposal – a temporary cessation against new names. Homo 60, 307–341. perspective. In: Otte, D., Endler, J.A. (Eds.), Speciation and its Consequences. Rak, Y., 1990. On the differences between two pelvises of mousterian context from Sinauer, Sunderland, Massachusetts, pp. 3–27. the Qafzeh and Kebara Caves, Israel. Am. J. Phys. Anthropol. 81, 323–332. Templeton, A.R., 1998. Species and speciation: geography, population structure, Rak, Y., 1993. Morphological variation in Homo neanderthalensis and Homo sapiens ecology, and gene trees. In: Howard, D.J., Berloche, S.H. (Eds.), Endless Forms: in the Levant: a biogeographic model. In: Kimbel, W.H., Martin, L.B. (Eds.), Species and Speciation. Oxford University Press, New York, pp. 32–43. Species, Species Concepts, and Primate Evolution. Plenum Press, New York, pp. Templeton, A.R., 1999. Human races: A genetic and evolutionary perspective. Am. 523–536. Anthropol. 100, 632–650. 50 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Templeton, A.R., 2005. Haplotype trees and modern human origins. Yearbook Phys. Wall, J.D., Yang, M.A., Jay, F., Kim, S.K., Durand, E.Y., Stevison, L.S., Gignoux, C., Anthropol. 48, 33–59. Woerner, A., Hammer, M.F., Slatkin, M., 2013. Higher levels of Neanderthal Tetushkin, E.Y., 2001. Genetics and the origin of human ‘‘races’’. Russ. J. Genet. 37, ancestry in East Asians than in Europeans. Genetics 194, 199–209. 853–867. Webster, M.T., 2009. Patterns of autosomal divergence between the human and Trinkaus, E., 2005. Early modern humans. Annu. Rev. Anthropol. 34, 207–230. chimpanzee genomes support an allopatric model of speciation. Gene 443, 70–75. Trinkaus, E., 2007. European early modern humans and the fate of the Neanderthals. Wiens, J.J., Servedio, M.R., 2000. Species delimitation in systematics: inferring Proc. Natl. Acad. Sci. 104, 7367–7372. diagnostic differences between species. Proc. R. Soc. Lond. B 267, 631–636. Trinkaus, E., Duarte, C., 2000. The hybrid child from Portugal. Sci. Am. 282, 102–103. Wild, E.M., Teschler-Nicola, M., Kutschera, W., Steier, P., Trinkaus, E., Wanek, W., Trinkaus, E., Moldovan, O., Milota, Sß., Bîlga˘r, A., Sarcina, L., Athreya, S., Bailey, S.E., 2005. Direct dating of Early Upper Palaeolithic human remains from Mladecˇ. Rodrigo, R., Mircea, G., Higham, T., Ramsey, C.B., van der Plicht, J., 2003. An early Nature 435, 332–335. modern human from the Pesßtera cu Oase, Romania. Proc. Natl. Acad. Sci. 100, Wiley, E.O., 1978. The evolutionary species concept reconsidered. Syst. Zool. 27, 17– 11231–11236. 26. Valdiosera, C., García, N., Dalén, L., Kahlke, R.-D., Lidén, K., Angerbjörn, A., Arsuaga, Wolpoff, M.H., Frayer, D.W., Jelínek, J., 2006. Aurignacian female crania and teeth J.L., Götherström, A., 2006. Typing single polymorphic nucleotides in from the Mladecˇ caves, Moravia, Czech Republic. In: Tescheler-Nicola, M. (Ed.), mitochondrial DNA as a way to access Middle Pleistocene DNA. Biol. Lett. 2, Early Modern Humans at the Moravian Gate: The Mladecˇ Caves and Their 601–603. Remains. Springer, Vienna, pp. 273–340. Van Valen, L., 1976. Ecological species, multispecies, and oaks. Taxon 25, 233–239. Wood, B., Lonergan, N., 2008. The hominin fossil record: taxa, grades and . J. Vernot, B., Akey, J.M., 2014. Resurrecting surviving neandertal lineages from Anat. 212, 354–376. modern human genomes. Science 343, 1017–1021. Wood, B.A., Richmond, B.G., 2000. Human evolution taxonomy and paleobiology. J. Wakeley, J., 2008. Complex speciation of humans and chimpanzees. Nature 452, E3– Anat. 197, 19–60. E4. Yang, M.A., Malaspinas, A.-S., Durand, E.Y., Slatkin, M., 2012. Ancient structure in Wall, J.D., 2000. Detecting ancient admixture in humans using sequence Africa unlikely to explain Neanderthal and Non-African genetic similarity. Mol. polymorphism data. Genetics 154, 1271–1279. Biol. Evol. 29, 2987–2995. Wall, J.D., Lohmueller, K.E., Plagnol, V., 2009. Detecting ancient admixture and Yokley, T.R., Churchill, S.E., 2006. Archaic and modern human distal humeral estimating demographic parameters in multiple human populations. Mol. Biol. morphology. J. Hum. Evol. 51, 603–616. Evol. 26, 1823–1827.