Primate model

Journal of Anthropological Archaeology 35 (2014) 32–50

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Journal of Anthropological Archaeology

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / j a a

The place of the Neanderthals in hominin phylogeny

http://dx.doi.org/10.1016/j.jaa.2014.04.004 0278-4165/� 2014 Elsevier Inc. All rights reserved.

⇑ Corresponding author. E-mail address: [email protected] (M. Grove).

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

a r t i c l e i n f o a b s t r a c t

Article history: Received 8 May 2013 Revision received 21 March 2014 Available online 13 May 2014

Keywords: Neanderthals Taxonomy Species status

Debate over the taxonomic status of the Neanderthals has been incessant since the initial discovery of the type specimens, with some arguing they should be included within our species (i.e. Homo sapiens nean- derthalensis) and others believing them to be different enough to constitute their own species (Homo neanderthalensis). This synthesis addresses the process of speciation as well as incorporating information on the differences between species and subspecies, and the criteria used for discriminating between the two. It also analyses the evidence for Neanderthal–AMH hybrids, and their relevance to the species 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 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.

� 2014 Elsevier Inc. All rights reserved.

Introduction

Neanderthals were given the Linnaean name of Homo neander- thalensis after King’s (1864) description of the original type-speci- mens, which he felt were so different from modern Homo sapiens that they may even represent a new genus. King’s (1864)view con- trasts with Huxley’s (1863) classification of Neanderthals as a sub- species of human (Homo sapiens neanderthalensis), owing to the latter’s belief that they could be included in Linnaeus’ (1802) H. sapiens despite their primitive nature (Tattersall, 2007). The debate continues into modern research, with some believing Neanderthals are sufficiently differentiated to constitute a separate species (e.g. Tattersall, 1986; Holliday, 2006), and others disagreeing (e.g. Dobzhansky, 1944; Currat and Excoffier, 2004). A recent preference for the species classification has arisen (de Vos, 2009), although a group of recent papers using studies of the Neanderthal genome (Green et al., 2010; Mendez et al., 2012; Wall et al., 2013) strongly indicating interbreeding between Anatomically Modern Humans (henceforth AMH) and Neanderthals, has re-awakened the debate.

There is a very real need to return to the rules and methods of traditional taxonomy to further our understanding of what 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- sal patterns found in all species, and thus have to be applicable, despite inherent anthropocentrism and a subsequent belief that

AMH are innately different to other organisms. This article aims to draw from taxonomic biology, identifying the methods of distin- guishing species and subspecies before assessing the relevant mor- phological and genetic evidence, as well as the supposed direct evidence of interbreeding between these two populations in the form of hybrids.

The species ‘problem’

The ‘species problem’ is largely a result of the philosophy and history of the field of taxonomy (Ghiselin, 1974). The main issues can be assigned to three categories: definition and concepts of what constitutes a ‘species’; the speciation process; and debates concerning criteria for species identification (Simpson, 1961; de Queiroz, 2005). While species are fundamental to the study of evo- lution (Tattersall, 1986), they are considered by some to be arbi- trary (Dobzhansky, 1935; Foley, 1991), and to lack a single reality over a geographic and temporal range (Simpson, 1951; Foley, 1991; Mallet, 2007).

Definition of ‘species’

The first problem lies in an inconsistency in the use and meaning of the term ‘species’. Different definitions include: a rank in a Lin- naean hierarchy using individual attributes to encompass all organ- isms at the species level (Quicke, 1993; Mayr, 1996), the end product of speciation (Nixon and Wheeler, 1990; Shaw, 1998), or the concept of what it is to be a species and what this category

S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 33

represents (Kimbel and Rak, 1993; de Queiroz, 1998). Issues arise over the inherent tautology of definitions, with species frequently being defined as ‘whatever a competent taxonomist says is a spe- cies’ (Quicke, 1993).

The nature and definition of species is intimately linked to the process of speciation, as species are dynamic parts of this overall process (Harrison, 1998) and can therefore only be an abstract cat- egory (Dobzhansky, 1935). Speciation in mammals is a gradual process not an instantaneous event (Simpson, 1951; Mayr and Ashlock, 1991; de Queiroz, 1998), which means we should expect to find organisms representing the entire panoply of stages, not just the end product (Mayr, 1964, 1996; Mayr and Ashlock, 1991). Five such stages have been proposed for gradualistic speci- ation: local populations, subspecies, semi-species, sibling species, and morphologically different species (Masters, 1993), yet distin- guishing between these stages is more difficult.

Species concepts

Most debate is over the true ‘concept’ of species (Hey, 2006), as frameworks for study and identification of species are dependent on the researcher’s species concept (Quintyn, 2009). All concepts are arbitrary to some extent (Reydon, 2004), with different con- cepts producing different numbers of taxa (Foley, 1991; Balakrishnan, 2005). Some have argued that the ‘Species Concept’ problem is itself a fallacy, as all researchers seem to agree on one concept in the linguistic sense at least, with species being the tip of an evolutionary lineage (Hey, 2006). Fig. 1 gives an indication of the complex development of this area of the philosophy of tax- onomy, with the number of current species concepts being at least

Fig. 1. ‘Phylogeny’ of species con

23 (Quintyn, 2009). The eight main concepts with relevance to this matter are summarised in Appendix A.

The definitions of species provided by the Phylogenetic and Evolutionary Species Concepts are readily applicable to the Nean- derthal species debate, and would support species status in the sense that there is a consistent use of morphology to identify Nean- derthal specimens and that this population eventually arrived at extinction. The Recognition Concept (Paterson, 1981) identifies species through species-specific mating recognition systems (SMRS), which have been tentatively inferred in fossil hominins. For instance, as Neanderthals and AMH are clearly different in appearance to palaeoanthropologists, they must at least represent different subspecies (Tattersall, 1992). However this concept has been said to overestimate (Tattersall, 1992) or underestimate (Kimbel, 1991) the number of species, as hominid skeletons do not have obvious morphological features that can be linked to SMRS (Kimbel, 1991), and its tautological nature has been revealed upon application to extant primates (Jolly, 1993).

Most debate over species classification uses the Biological Spe- cies Concept proposed by Mayr (1964) and Dobzhansky (1935), which defines species as reproductively isolated populations. According to the criterion of complete reproductive isolation, Neanderthals and AMH would have to be classified as the same species if interbreeding did occur. Yet this strict criterion was objected to by both Darwin and Wallace. Wallace took his objec- tion further by highlighting the circular reasoning of defining and delimiting a taxon by the same criteria (Mallet, 1995). The require- ment of complete reproductive isolation is a common misconcep- tion: Mayr himself acknowledged that occasional hybridisation occurs between sympatric species (Mayr, 1964, 1996), as isolation mechanisms do not prevent all interbreeding, with their main role

cepts (Quintyn, 2009: 310).

Table 1 Four classes of subspecies definitions (Long and Kittles, 2003, p. 468).

Class Definition

Essentialist – Share a combination of derived traits – Features more or less obscured by individual variations

Taxonomic – Aggregate populations sharing phenotypic similarities – Inhabit geographic subdivision of range of the species – Differ taxonomically from other intraspecific populations

Population – Genetically differentiated and distinct Mendelian populations – Consist of genetically differentiated individuals

Lineage – A distinct evolutionary lineage within a species – Genetically differentiated due to barriers to genetic exchange over time – Historical continuity and genetic differentiation

34 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

being protection of a harmonious gene pool (Mayr, 1996). As shall be shown, interbreeding freely occurs between different taxo- nomic levels without compromising species status. Most accept the main principles of this concept and use it to provide practical guidelines (Tattersall, 1992), overcoming the main issues by mod- ifying and supplementing this concept with other, more appropri- ate concepts (Simpson, 1951).

Species criteria and methods of delimitation

Criteria used to delineate species boundaries inevitably arise from the Species Concept that is being applied (Quintyn, 2009). There are fundamental problems with creation of appropriate cri- teria, mainly due to the occurrence of mosaic evolution, with dif- ferent characteristics evolving at different rates (Mayr, 1996). Taxonomy largely depends on morphological characteristics (Simpson, 1961; Smith, 1994; Mayr, 1996), despite an indirect rela- tionship between morphology and genetics (through reproductive isolation) (Simpson, 1961; Mayr and Ashlock, 1991). This, accom- panied by inapplicability of many species ‘criteria’ to fossil samples (Tattersall, 1986) and small sample bases (Simpson, 1961), compli- cates the practice of species delineation, especially when consider- ing the Biological Species Concept.

Despite these inherent problems, certain criteria are regularly used, including:

– Reproductive isolation (Simpson, 1951; Harrison, 1998) which can involve: � Genetic exclusivity (Harrison, 1998). � Genotypic clusters (Harrison, 1998).

– Morphological divergence (Simpson, 1951) potentially leading to: � Autapomorphies (Nixon and Wheeler, 1990). � Fixation of characters (Kimbel and Rak, 1993).

– Ecological distinctiveness (Simpson, 1951; Harrison, 1998). – Separate evolutionary identities and tendencies (Simpson,

1951; Harrison, 1998).

All species criteria require some level of qualitative, subjective judgement (Sites and Marshall, 2004). For instance interbreeding, where Mayr himself (Mayr, 1964), along with many others (Simpson, 1951; Harrison, 1998) acknowledges that interbreeding may occur between populations that nevertheless retain their genetic and morphological identities. This criterion cannot be used in isolation (Mayr, 1964), and should be considered as a sufficient indication of species status, rather than a necessary criterion (Balakrishnan, 2005). Genetic criteria have their associated issues, with their validity under constant debate (Masters, 1993). Morpho- logical criteria require an arbitrary level for a ‘sufficient’ level of divergence (Sites and Marshall, 2004), as does character fixation, where ‘true’ (100%) fixation is statistically impossible to prove (Wiens and Servedio, 2000).

Traditional taxonomy

Traditional taxonomy could be said to use primarily the Typo- logical Species Concept (Mayr, 1996; Boggs, 2001), based upon Lin- naeus’ own idea of species as static groups forming the lowest category in his hierarchy (Mayr and Ashlock, 1991; Tattersall, 1992), marked by sharp discontinuity (Mayr and Ashlock, 1991) and representing divine origin (Mayr, 1964). This idea has been lar- gely rejected by many researchers, owing to the problems that arise in polytypic species (Mayr and Ashlock, 1991). Instead, the modern typological concept defines species as a ‘class of individu- als sharing defining attributes’ (Boggs, 2001). It has the advantage

that it can be applied to most cases, but involves a subjective deci- sion over which traits to use (Boggs, 2001).

As can be seen, the primary criteria (for fossils at least) are mor- phological, with the assumption being that morphology approxi- mates genetic differences (Simpson, 1943). This ‘morphospecies’ concept is the main method used in palaeontological taxonomy (Holliday, 2003) due to its practicality. However the evolutionary meaning of such groups is speculative at best (Holliday, 2003; Ahern, 2006). In addition, the indirect relationship between mor- phology and speciation (Foley, 1991; Mayr, 1996; Tattersall and Schwartz, 2006) invalidates the original assumption, although counterarguments allege that morphological differences should suggest absence of reproductive isolation (Simpson, 1951; Wiens and Servedio, 2000). Morphological criteria are, again, subjective and could ignore the evolutionary significance of species (Simpson, 1951). Nevertheless, such methods have some efficacy, as behaviour and morphology could be considered more relevant to the production of species than genetic differences (Mallet, 2007), and morphology at least provides a clear method for species demarcation (Mayr, 1996).

Subspecies

Subspecies can be defined as a group of organisms in which interbreeding with other subspecies occurs regularly (Simpson, 1943), with each variant normally marked by significant morpho- logical differences (Keita et al., 2004). Genetically, subspecies exist as open systems (Dobzhansky, 1935) which may intergrade almost unnoticeably (Mayr, 1964) or be separated by a migration barrier (Livingstone and Dobzhansky, 1962). Four different definitions exist, summarised in Table 1. There is a trend towards the rejection of the term in scientific circles due to its ability to obscure the more important relationships between members of populations (Gould, 1991), and application requires a minimum threshold of difference, as each population will have developed some genetic or morphological characteristic by which they could be distin- guished from other groups (Templeton, 1999).

The subspecies taxon is relatively more arbitrary than that of species (Tetushkin, 2001), although Livingstone and Dobzhansky (1962) have argued that the naming and identification are subjec- tive, whereas their existence is indisputable. Identification requires a large series of comparisons over the geographic range of the spe- cies (Mayr, 1964), posing immediate problems for identification in the archaeological record. Methods can be made more objective, for example through the 75% rule where over 75% of a subspecies should be distinguishable by diagnostic characters (Mayr, 1964), or more subjective, where contemporaneous subgroups in a larger morphological group may be distinguishable (Simpson, 1943). There are no agreed criteria for distinguishing subspecies (Long and Kittles, 2003), with the main criterion being whether the

Table 2 Five types of allopatry (Mayr et al., 1953).

S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 35

intraspecific variation is greater than interspecific variation among groups (Long and Kittles, 2003).

Contact Interbreeding Zone of contact

Taxonomic classification

1 In contact – Intergradation/ interbreeding in zone of contact

Fairly wide – Same species – Subspecies status dependent on degree of difference

2 In contact – Interbreed completely in zone of contact

Narrow – Same species – Subspecies

3 In contact – Do not interbreed freely

– Separate, full species

– Occasional hybrids

4 In contact – No interbreeding – Full species – Reproductive isolation

5 Separated – No interbreeding Distributional gap

– Unsure – Use morphology to infer taxonomic status – Preferable to treat as subspecies

Hybridisation

The definition of hybridisation that will be used is ‘‘interbreed- ing between individuals from genetically differentiated lineages over a wide range of taxonomic levels’’ (Jolly, 2001; Ackermann, 2010). This process has been largely ignored or misunderstood, possibly due to the nature of cladistics itself, which is inherently ineffective at identifying hybridisation (Holliday, 2003). However, Jolly (2001) has demonstrated how the acceptance of hybridisation can facilitate greater parsimony in cladistic phylogeny. Hybridisa- tion is widespread in many groups of animals (Ackermann, 2010). Among primates, hybridisation occurs in Cercopithecidae (Cortés- Ortiz et al., 2007), Papionins (Jolly, 2001; Arnold and Meyer, 2006; Burrell et al., 2009), Gibbons (Arnold and Meyer, 2006), Orang-utans (Arnold and Meyer, 2006), Gorillas (Ackermann and Bishop, 2009), and Chimpanzees (Arnold and Meyer, 2006). Con- sidering this widespread occurrence in the Primate order and the close genetic relationship between members of the Hominini (Holliday, 2003), the assumption that hybridisation did not occur during hominin evolution is questionable and is likely to lead to inaccuracies in reconstruction.

Speciation is generally considered to be gradual process that can take between 2 and 4 Ma (Ackermann, 2010), with hybrid invi- ability in mammals occurring at the end of this process (Fitzpatrick, 2004). Post-zygotic isolating mechanisms in mammals evolve over much longer timescales than behavioural or morpho- logical differentiation, meaning that if taxa meet after experiencing significant periods of isolation, reproduction could occur if not pre- vented by pre-zygotic isolating mechanisms (Grant and Grant, 1998; Holliday, 2006). A strongly relevant example is the high probability of gene exchange between human and chimpanzee ancestors up to 4 Ma after their initial divergence (Bower, 2006; Patterson et al., 2006; but see Wakeley, 2008; Webster, 2009), and another is the documented hybridisation between Alouatta palliate and Alouatta pigra, species that diverged over 6 Ma (Arnold and Meyer, 2006). Holliday (2006) found that 172 out of 328 documented occurrences of hybridisations between taxo- nomic species produce fertile, viable offspring. Considering the evi- dence, later Homo sp. could be said to be members of a syngameon, a term introduced by Lotsy (1925) referring to a larger group of species capable of successful hybridisation (Holliday, 2006).

The BSC incorporates a certain level of hybridisation, demon- strated by Mayr’s discussion of the five different kinds of allopatry (shown in Table 2) in relation to interbreeding and taxonomic clas- sification, which shows that separate species can be capable of interbreeding in certain circumstances. The Neanderthal–AMH interaction could be characterised as either condition 2, 3 or 4. In general, the conclusion that hybridisation between AMHs and Neanderthals would indicate the conspecificity of these groups is false (Ackermann, 2010) and a result of misdirected application of the species concept (Hey et al., 2003; Arnold and Meyer, 2006). The ‘issue’ of hybridisation does not exist, if one defines spe- cies as lineages remaining cohesive despite occasional genetic exchange (Holliday, 2003).

Very low levels of interbreeding are required for favourable genes to spread between taxa (Barton, 2006) even if selection against hybrids occurs (Holliday, 2006) with the only requirement being that at least some of the hybrids are partially viable and fer- tile (Jolly, 2001). In fact, genes introduced through hybridisation could have a higher probability of spreading through a population’s genome due to the nature of hybridisation. These genes, unlike those arising through mutation, have been subject to selection

within their original genome, and are therefore unlikely to be lethal. If they are disadvantageous they may be removed by the process of natural selection, meaning that they have a higher prob- ability of being advantageous. This in turn means that those genes which are mutually advantageous to both hybridising populations could rapidly reach fixation (Jolly, 2001). In relation to Neander- thal–AMH hybridisation, Jolly (2001) argued the issue of whether genetic evidence would survive in the face of the effects of later colonisation and genetic drift (Jolly, 2001): the recent studies of the Neanderthal genome indicate that it may do so (Green et al., 2010; Mendez et al., 2012; Wall et al., 2013).

Recognising hybridisation in the fossil record

We have little knowledge of what a hybrid fossil would look like (Ackermann, 2010), with Jolly (2001: 190) stressing the ‘‘vanish- ingly small’’ chances of recognising a Neanderthal–AMH hybrid. This position is the result of our lack of knowledge about the effect of genetic introgression on the phenotype and the validity of the assumption that such genes will be directly linked to morphology (Jolly, 2001; Ackermann, 2010). The uncertainty is exacerbated by the fact that the fossil evidence is likely to underestimate physical differences between specimens (‘Tattersall’s Law’) (Tattersall, 1993), and Jolly’s (2001) study of Papionin hybridisation empha- sises the point. Beyond question we are restricted by the absence of soft-tissue characteristics as well as the small samples available from an incomplete fossil record (Ackermann, 2010).

Jolly has emphasised the consequent need to rely on analogies, for instance his direct analogy of the relationship between Hama- dryas (Papio hamadryas) and Anubis (Papio anubis) baboons, which produce natural hybrids after a divergence time of 600 Ka (Jolly, 2001). Such comparisons demonstrate that the assumed pattern of intermediate morphology is only one of many possible out- comes, including: cryptic hybrids (those indistinguishable from one of the parental taxa), transgressive hybrids (those showing variation outside of the range of the parental taxa) and hybrids with phenotypes closer to one parental taxon rather than the other (Ackermann, 2010). Possible indicators could include intermediate characteristics, rare anomalies, or complicated patterns of synapo- morphies and high levels of individual variability (Harvati et al., 2007; Ackermann and Bishop, 2009; Ackermann, 2010), although these are features observed in hybrids of different genera and may be less applicable to hominins.

36 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Evidence of Neanderthal–AMH hybrids

The possibility of Neanderthal–AMH hybrids has long been recognised, for instance with Dobzhansky’s (1944) proposition that the Mount Carmel specimens could indicate subspecific hybridisa- tion (Grant and Grant, 1998). Other examples analysed by Grant and Grant (1998) include some Krapina specimens, dated to 130 Ka, which display one of the aforementioned criteria of hybrid- isation: high occurrence of an unusual trait in the form of a rotated third premolar (36% in these specimens versus a normal rate of 6% in Neanderthals and AMH). Three specimens from Qafzeh, along with Skhul IV and Amud 1 also demonstrate dental anomalies (Grant and Grant, 1998), and all occur in a supposed region of con- tact between H. sapiens and H. neanderthalensis, supporting their potential hybrid status.

There are multiple later examples of potential hybrids in Eur- ope, mostly dating to the period when H. sapiens are known to be entering this area, allowing for the creation of a hybrid zone. The specific morphological characteristics are summarised in Table 3, but here the focus is laid on a few key specimens. The first is the well-known ‘hybrid child’ of Abrigo do Lagar Velho, dated to 24.5 B.P. (Duarte et al., 1999). Despite displaying a mixture of fea- tures that led some to conclude it has hybrid status (Duarte et al., 1999; Trinkaus and Duarte, 2000), Tattersall and Schwartz (1999) have emphasised that this F1-typical (first generation) mixture is not to be expected hundreds of generations after initial hybridisa- tion, proposed to have occurred around 30 ka (Trinkaus and Duarte, 2000). More refined dating applications suggest that Nean- derthals disappeared from Iberia earlier than some radiocarbon dates had indicated, perhaps as much as 40 ka (Higham et al., 2006), but they do not affect the point that Lagar Velho is unlikely to belong with the first contacts. Holliday (2006) has also observed that the existence of F1 hybrids in a hybrid zone is relatively rare, which decreases the likelihood of discovering such a rare hybrid in the fossil record.

The Vindija specimens, dated to between 33 and 40 ka (Krings et al., 2000; Higham et al., 2006) are generally accepted as H. nean- derthalensis, although some intermediate features could indicate a mixed ancestry (Ahern et al., 2002). Some have argued that this would indicate the presence of hybridisation (Ahern et al., 2002), whereas others have commented that individuals such as those from Vindija could be Neanderthals independently evolving a mor- phology similar to that seen in the AMH trajectory (Delson et al., 2000). Such homoplasy could have arisen between the two lin- eages due to phenotypic plasticity, where European Neanderthal morphology may have been responding to similar environmental pressures to AMH.

Morphological assessment

As has been noted, morphology is the most common method for taxonomic assignation in hominin palaeontology. To reduce or eliminate subjectivity, comparative methods are employed to define levels of expected intraspecific and inter- specific variation in morphological traits of living species (Mayr and Ashlock, 1991; Tattersall, 1986; Harvati, 2003). Although this method is more complicated and results in less certain conclusions, it is the only relatively objective and satis- factory method that can be applied to morphology. There is a clear lack of a closely-related out-group for comparative analy- ses. Chimpanzees, our closest living relative, do not represent a valid candidate, due to the large evolutionary gap between them and hominins and the possibility that they may have undergone a different pattern of morphological differentiation (Harvati, 2003).

AMH versus Neanderthals

AMH are more difficult to define in terms of their characteristic morphology than Neanderthals (Wood and Richmond, 2000). Table 4 lists some of the anatomical traits that can be used to dis- tinguish this morphospecies, yet most of these are defined in con- trast to Neanderthals. One example is the uniquely derived nature of H. sapiens frontal bone morphology, which can be used to iden- tify this group with high levels of accuracy (Arthreya, 2009). Despite this, Arthreya (2009) has also commented that the high level of intraspecific variation leads to difficulties in describing the specific features that make this species so morphologically distinct.

Tattersall (1986) has suggested that this high level of variation may in fact be interspecific: that H. sapiens could be an amalgam- ation of several separate species, with the ‘archaic’ and ‘anatomi- cally modern’ groups representing two of these. H. sapiens may be defined by symplesiomorphic, not synapomorphic features (Tattersall, 1992), and would therefore be cladistically unclassifi- able. In the light of this possibility, the belief that H. sapiens is actu- ally a subspecies could be seen as a gross misunderstanding of the levels of intraspecific variation that can be contained within one species.

Neanderthals can be more easily defined and diagnosed using their distinct morphological traits (Tattersall, 1992), as demon- strated by the list of Neanderthal characteristics in Table 5. Gener- ally Neanderthals are typified by increased robusticity and prominence of muscle attachment areas, with distinctive pelvis and rib cage morphology, low crural and brachial indices, and a particular combination of cranial features including occipital ‘bun- ning’ and midfacial prognathism. Neanderthals are associated with a specific combination of features and distinct general proportions and relationships between cranial areas (Tattersall and Schwartz, 1998), with the craniofacial differentiation in comparison to AMH being considered by some to correspond to species status (Harvati et al., 2004). Tattersall (2007) has even stated that this group is the most clearly demarcated extinct hominid group known as of yet, which would explain the frequent accurate differ- entiation of this group from other hominins by morphological assessment (Harvati, 2003).

This evidence would corroborate the classification of Neander- thals as a separate morphospecies (Harvati, 2003). Despite this, the question remains as to whether the listed traits are synapo- morphic, autapomorphic or symplesiomorphic. Tattersall (1992) and Kimbel (1991) have argued for the highly autapomorphic nat- ure of Neanderthals. Demonstrably derived features include 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 AMH bear closer resemblance to Homo erectus than Neanderthals do. The case is even stronger for the derived nature of Neanderthal elbow morphology, with AMH morphology being more similar to that of the australopithecines (Yokley and Churchill, 2006).

Neanderthals inevitably retain some symplesiomorphic fea- tures, for instance large supraorbital tori, a low cranial vault (Santa Luca, 1978) and aspects of the pelvis (Rak, 1993). These are not unexpected, and evidence evolutionary relationships such as those between Neanderthals and the Steinheim and Sima de los Huesos specimens (Wood and Richmond, 2000; Tattersall, 2007). The characteristics shared with AMH merely demonstrate their relationship as sister taxa and the fact that they were gener- ally synchronic and sympatric groups (Holliday, 2003), and there- fore could be homoplastic (Stringer and Andrews, 1988). This point is also indicated by the large amount of intraspecific variation found in both groups (Tattersall and Schwartz, 2006; Arthreya, 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 and Schwartz, 1998). Comparisons with other closely-related mammalian species show that minimal differentiation and large overlap in hard-tissue characteristics are the norm (Tattersall, 1986; Tattersall and Schwartz, 1998), with differences between subspecies of primates being comparatively tiny (Tattersall, 1986).

The morphological evidence leads to one conclusion, that Nean- derthals and AMH represent distinct species. Neanderthals in par- ticular are a distinctive, cohesive evolutionary group (Santa Luca, 1978; Tattersall and Schwartz, 1998). The most important point to note is the clear hiatus between the Neanderthal and AMH mor- phologies (Santa Luca, 1978). The comparative difference between Neanderthals and AMH is at least as great as that between closely- related extant species (Tattersall, 1986), and in the case of cranio- dental evidence, larger (Tattersall, 1992). Harvati’s comparison of intraspecific and interspecific variation with chimpanzee species has led to a similar conclusion: the difference between Neander- thals and AMH is greater than AMH intraspecific variation, and greater than the distance between Pan paniscus and Pan troglodytes (Harvati, 2003). As the majority of morphological change in a line- age is expected to arise after the true speciation event, even incip- ient Neanderthal features would be sufficient to conclude separate species status (Rak, 1993).

Genetic evidence

Enormous progress has been made in the last twenty years in the recovery of genetic evidence from bone (Pääbo, 2003; Green et al., 2006, 2010; Valdiosera et al., 2006; Meyer et al., 2012; Dabney et al., 2013), considerably reshaping views of human evo- lution through the last half million years. There remain numerous problems associated with DNA studies into Neanderthal introgres- sion, although it must be admitted that very rapid progress in development of techniques will much reduce these. Obvious sources of error include contamination from modern human DNA, which is pervasive in archaeological remains (Serre et al., 2004; Serre and Pääbo, 2006), and exacerbated by the damaged nature and small samples of Neanderthal DNA (Green et al., 2009). This difficulty is coupled with the overwhelming similarity of Neanderthal and AMH DNA (Serre and Pääbo, 2006; Green et al., 2008, 2009), often leading to AMH-like DNA sequences being taken as evidence of contamination rather than introgression (Serre et al., 2004).

DNA analyses depend on estimates of the population size of the invading H. sapiens population (Forhan et al., 2008) and genetic diversity, both of which may have been variable and are difficult to estimate (Wall, 2000). There is a high probability that both Neanderthals (Orlando et al., 2006; Dalén et al., 2012) and AMH (Loogväli et al., 2009; Wall et al., 2009) underwent significant pop- ulation and genetic bottlenecks, which could explain the reduced genetic diversity of later Neanderthals (Krings et al., 2000; Serre and Pääbo, 2006), although the results of the study of Lalueza- Fox et al. (2005) would contradict this bottleneck hypothesis. Alves et al. (2012) have even suggested that admixture would have a significant effect on such estimates of AMH demography.

Issues also exist in the data sets used, as most comparative AMH DNA is from modern individuals, yet later effects such as drift and genetic ‘swamping’ could eliminate traces of earlier introgression (Serre and Pääbo, 2006), so that larger samples of Upper Palaeolith- ic AMH DNA would be required for gaining a more balanced pic- ture (Nordberg, 1998; Serre et al., 2004). It is unlikely that we shall retrieve sufficient DNA from the common ancestral species (Lindahl, 1997; Krings et al., 2006) which limits us to estimations of the symplesiomorphic genome. Early samples were of small DNA fragments from few individuals (Serre and Pääbo, 2006),

which could affect estimates of genetic diversity (Briggs et al., 2009), yet the recent application of a high coverage method (Max Planck Institute for Evolutionary Anthropology, 2013) also employed by Meyer et al. (2012) for Denisovan material, could resolve this issue in the future.

As in morphological analysis, single genetic synapomorphies can theoretically be used to define phylogenetic relationships, but this is only possible in rare situations (Knight, 2003), necessi- tating in-depth study to reveal interactions between Neanderthals and AMH. The identification of hybridisation through DNA analysis is theoretically possible, with hybrid DNA showing different diver- gence times in comparable regions of the genome (Lalueza-Fox et al., 2012), yet can be complicated by numerous factors, which are treated here briefly.

Mitochondrial DNA evidence

Early genetic studies were based on the analysis of mitochon- drial DNA (mtDNA). MtDNA is particularly useful for ancient DNA studies due to its relative abundance and increased likelihood of retrieval (Endicott et al., 2010), as well as the fact that it is maternally inherited (Giles et al., 1980) and thus non-recombining (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., 2005; Lalueza-Fox et al., 2005, 2006; Caramelli et al., 2006; Noonan et al., 2006; Orlando et al., 2006; Serre and Pääbo, 2006; Green et al., 2008; Briggs et al., 2009), and 8 AMHs (Scholz et al., 2000; Caramelli et al., 2003; Serre et al., 2004; Pettitt, 2011) has been analysed. Most compare Neanderthal evidence with modern mtDNA, but signals of admixture may have been affected by later genetic bottlenecks and drift, necessitating comparison with pre- historic AMH DNA.

Such studies conclude that Neanderthal DNA clusters to the exclusion of modern humans (Krings et al., 2000; Knight, 2003), with the overall difference between the two populations being three times as great as the intraspecific mtDNA variation for mod- ern humans (O’Rourke et al., 2000; Tetushkin, 2001) and half of that between modern humans and chimpanzees (O’Rourke et al., 2000). This finding leads to the conclusion that no introgression occurred (Tetushkin, 2001), supported by the lack of any direct evi- dence of introgressed genes.

If the absence of evidence of introgression is a true reflection of the prehistoric situation, it would limit the possible amount of admixture that occurred (Krings et al., 2006), with maximum esti- mates ranging from 0.1% to 25% (Forhan et al., 2008) and minimum estimates of 0 (Ghirotto et al., 2011). Yet there are many issues associated with mtDNA analyses, including frequent introgression of mtDNA across species boundaries (Barton, 2006), dependencies on estimates of mutation rates (Hawks, 2006), and questionable claims of the selective neutrality of mtDNA (Nordberg, 1998; Hawks, 2006). A negative consequence of the maternal inheritance of mtDNA is that such sequences cannot reveal the entire evolu- tionary history of a population (Templeton, 2005), meaning that nuclear DNA analyses are required to corroborate the conclusion of an absence of Neanderthal–AMH admixture (Beerli and Edwards, 2002; Lalueza-Fox et al., 2012).

Nuclear DNA evidence

The main results of the Neanderthal genome study were first published by Green et al. (2010), who used a new measure, the D statistic, and concluded that introgression of Neanderthal genes into the AMH genome of between 1.3% and 2.7% must have occurred due to the fact that Neanderthal DNA was closer to that of non-Africans than to that of Africans. They argue that, as

Table 3 Review of possible Neanderthal–AMH hybrids.

Site Date H. neanderthalensis features H. sapiens features Intermediate/anomalous features

Taxonomic assignation

Cioclovina, Romania

29–210 kya (33.2– 33.8 kya BP cal)q

– Supraorbital torih,o

Suprainiac fossap,q

– Nuchal torusp,q

– External occipital protuberanceq

– Occipital ‘hemi-bun’p

– Supraorbital tori not continuousq

– Superior nuchal lines (position and size)q

– High, vertically rising frontal 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

H. sapiensh,q

Abrigo do Lagar Velho, Portugal

25.6 kyaf – Juxtamastoid eminencei

– I2 shovelling i

– Suprainiac fossai

– Juxtamastoid eminencef

– Posterior retreat of mandibular symphysisf,i

– Dental maturational patternc

– Anterior symphyseal configuration of the mandiblef

– Femoral midshaft circumference versus lengthf

– Proximal humeral diaphyseal morphologyf

– Strongly developed pectoral musclesf

– Short, stout legsr

– Backwards sloping of mandibler

– Limb segment proportionso

– Development of ‘‘chin’’f,r

– I2 breadth f

– Breadths of I2 versus Ms f

– Anteromedial position of radial tuberosityf

– Little lateral curvature of the radiusf

– Small front teethr

– Short facer

– Minimal brow developmentr

– Narrow anterior pelvisr

– Size of juxtamastoid processf

– Size of mastoid processf

– Hybridf,r

– Possible hybrid?k

– H. sapiensc

Mladeč 1 and 2 (females)

31 kyat – Pronounced occipital ‘bun’t

– Distinctive nuchal areat

– Large juxtamastoid eminencesp

– High foreheadt

– Reduced browst

– Small facial dimensionst

– H. sapiens?d,t

Mladeč 3 (infant) 31 kyat – Thick, well-developed medial brow ridgesj

– Prominent glabellaj

– Strongly developed occipital bunj,p

– Low occipital heightj

– Lambdoid flatteningj

– Short occipital plane lengthj

– Short and low temporal bonej

– Prominent juxtamastoid eminencej

– Shape of orbitj

– Degree of frontal vaultingj

– Antero-superior orientation of the external auditory meatusj

– Strongly concave glenoid fossaj

– Post-glenoid tuberclej

– Flat squamous temporalj

– Nuchal plane lengthj

– Occipital breadthj Hybridj

Mladeč 6, 7 and 9 (males)

31 kyat – Small mastoid processesg

– Lateral profileg

– Elliptical suprainiac fossaeg

– Shallow groove on inferior nasal marginsg

– Cranial height/length indexg

– Cranial breadthg

– Nasion projectiong

– Glabella projectiong

– ‘Square’ parietal bonesg

– Occipitomastoid crestg

– Supraorbital projectiong

– Supraorbital sulcusg

– Divergence of the temporal lineg

– Parietal thicknessg

– Occipital plane lengthg

– Mandibular fossag

– Strongly curved frontal boned

– Vertical heightg

– Supraorbital torus structureg

– Occipital (biasterionic) breadthg

– Possible hybrid?g

– Not hybridd

Pes�tera cu Oase, Oase 1 (mandible)

34–36 kyas – Unilateral bridging of mandibular forameno

– Mesial mental foramens

– Narrow lateral corpuss

– Absence of retromolar spaces

– Symmetrical mandibular incisuress

– Lateral incisures crests

– Small superior medial pterygoid tubercles

– Lingual bridging of the mandibular foramens

– Distal molar megadontias

H. sapienss

38 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

Table 3 (continued)

Site Date H. neanderthalensis features H. sapiens features Intermediate/anomalous features

Taxonomic assignation

Pes�tera cu Oase,Oase 2 (cranium)

36 kyal – Sagittal frontal arc (long and flat) l,p

– Large juxtamastoid eminencel

– Large buccolingual and mesiodistal diameters of molarsl

– Molar size progressionl

– Occipital ‘hemi-bun’p

– Overall cranial proportionsl

– Subrectangular orbitsl

– Infraorbital regions – pronounced canine fossael

– Modest superciliary archesl

– Narrow nasal aperturel

– No anterior mastoid tuberclel

– High, rounded parietal regionl,p

– Pentagonal contour in norma occipitalisl

– Unsure, possible hybridl

Pestera Muierii, Muierii 1

36 ky BP (cal)m – Frontal curvature of the neurocranial vaultm

– Shallow transverse suprainiac fossa m

– Median nuchal torusm

– Lacks retromolar spacem

– High coronoid processesm

– Asymmetrical notchesm,p

– Breadth/height index of scapular glenoid fossam

– Moderately low frontal arc of craniumm

– Occipital ‘bun’p

– Small superciliary archesm

– Deep canine fossaem

– Anterior zygomatic roots above M12

c

– Modest nasal aperture breadthm

– Dentitionm

– Scapulam

– Marked projection of the occipital bunm

Possible hybrida,m

Vindija, G1 29–210 kyab – Reduced midfacial prognathismb

– Reduced nasal breadthb

– Thinner cranial vaultsb

– Incipient chinsb

– Reduction and shape changes in supraorbital torusb

– Scapular glenoid fossae

– H. neanderthalensis?b

– Possible hybridb

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).

S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 39

Neanderthals are equally related to Chinese, Papua New Guineans and French, introgression must have occurred in the Middle East. Neves and Serva (2011) subsequently argued that the results need to be replicated before they can be accepted, preferably with larger samples of Neanderthal and Upper Palaeolithic nDNA, in view of the contradictory mtDNA evidence (Tetushkin, 2001; Krings et al., 2006). Nuclear DNA from the Vindija specimens had been analysed previously (see Serre et al., 2004; Noonan et al., 2006), however studies failed to find evidence of introgression.

An alternative explanation for Green et al.’s results might be that of ancient population substructure in AMH populations before they left Africa (Lalueza-Fox et al., 2012), with the African subpop- ulation that later gave rise to the dispersing AMHs sharing a longer ancestry with Neanderthals (Ghirotto et al., 2011). This point has been acknowledged by Green et al. (2010) and supported by the research of Wall et al. (2009) and analysis of the Xp21.1 gene (Garrigan et al., 2005). Durand et al. (2011) suggested that the D-

statistic would be confounded by such a population history, but conclude that admixture is a more parsimonious possibility than population substructure for the results of Green et al., and con- clude that tests could be used to eliminate substructure as an explanation. Similarly, Lohse and Frantz (2013) used a maximum likelihood method to reject population substructure as a cause of the genetic signatures found. Sankararaman et al. (2012) have made the lucid argument that, if interbreeding did occur after Neanderthals and AMH diverged, then genes would have been exchanged after �100 ka. If the substructure argument was valid, the date of the last genetic exchange would be closer to the date of common ancestry, around 230 ka (Sankararaman et al., 2012). As can be seen, there are ways to eliminate the explanation of sub- structure in this debate.

Many studies published since Green et al.’s (2010) paper have shown supporting evidence of introgression, frequently using divergent haplotypes (e.g. Abi-Rached et al., 2011) or patterns of

Table 4 List of AMH morphological characteristics.

Location Trait

Cranial traits

Calvarium Globular braincaseg

Short, high craniumf

Long, high parietal archf

Parietal arch – narrow inferiorly, broad superiorlyf

High frontal archf,g

Rounder frontal bonesa

Thin bones of cranial vaulte

Upper facial region

Discontinuous supraorbital torif

Reduction of supraorbital toria,e,g

Curved occipital bonef,f

Orthognathye

Nasal region Shorter nasion bregma chorda

Mandible Mental eminence (chin)f,g

Thin bone of mandibular bodye

Dental Anterior teeth Canine fossag

Postcanines Perfect oval shape of mandibular P4 b

Wide lingual crown of mandibular P4 b

Simplified occlusal morphologyg

Reduced crownsc,g

Reduced root sizec

Symmetrical lingual crown contourg

Absence of transverse crestg

Absence of accessory ridges and fissuresg

Reduction in number of cusps and rootsg

Absent or reduced metaconid forming a lingual shelfg

Postcranial Trunk Narrow trunkg

Limbs Elongated distal limbsg

Long limbs relative to trunkg

Small humeral bi-epicondylar breadthsh

Pelvis Short, stout pubic ramus with rounded cross- sectiond

Narrow pelvisg

General Low body mass relative to statureg

Loss of robusticitye,g

a Arthreya (2009). b Bailey and Lynch (2005). c Kupczik and Hublin (2010). d Rak (1990). e Stringer and Andrews (1988). f Tattersall (1992). g Wood and Richmond (2000). h Yokley and Churchill (2006).

Table 5 List of Neanderthal morphological characteristics.

Location Trait

Cranial traits Calvarium Smoothly rounded cranial profile from rear view (‘en bombe’)g,m,n,p

Lower cranial vaultd

Shorter, wider occipital planed

Suprainiac fossae,g,j,m,o,p

Rounded, laterally projecting parietal boner

Lambdoid flatteningo

Anteriorly placed lambdae

Occipital ‘bun’ (posteriorly projecting occipital)o,q,r

Horizontal occipital torus of uniform thicknessj,m

Occipital torus restricted to central part of occipital bonej,m

Angling along anterior squamosal suturen

Pronounced juxtamastoid eminenceg

Large juxtamastoid crestm

Smaller mastoid processd

Rounded mastoid protuberancej,m

Occipitomastoid process P mastoid process j,o

Upper facial region

Thick, double arched supraorbital torio,q,r

Supraorbital tori continuous across the glabellao

Inferomedially truncated orbitsn,p

Retreating zygomatic profilem,n,r

Long, thin zygomatic archesp

Pronounced midfacial prognathismd,g,m,r

Nasal region Well-developed medial projection of internal nasal margink

Swelling of lateral nasal cavitywallk

Capacious nasal aperturem,o

Large nasal fossao

Lateral expansion of the frontal sinuseso

Projecting nasal bonesm

Maxilla Underdeveloped mental eminenceo,r

Lack of ossified groove over lacrimal groovek

Narrow lower facen,o

Mandible Sigmoid notch crests terminate close to lateral ends of condylesn

Sigmoid notches deepest in front of low-set condylen,p

Obliquely truncated gonial anglesn

Inferior, lateral position of articular eminenced

Mental foramen under first mandibular molarr

Thin symphyseal bonep

Cranial base Wide sphenoid anglem

Highly pneumatised petrosal bonen,p

Long, narrow, ovoid foramen magnumn,p

Pronounced juxtamastoid eminenceg

Large juxtamastoid crestm

Smaller mastoid processd

Rounded mastoid protuberancej,m

Occipitomastoid process P mastoid processj,o

Bony labyrinth

Anterior semicircular arc

Relatively small and narrowl

Narrow in width relative to heightl

Posterior semicircular canal arc

Relatively smalll

Positioned more inferiorly relative to lateral canal placel

Lateral semicircular arc

Absolutely and relatively largel

Ampular line More vertically alignedl

Dental Anterior teeth

Broad anterior teetha,h,m,r

Shovelled incisorsa,f,h,r

Prominent lingual tuberclesa

Labial convexitya,f

Postcanines Relatively thin enamelh

Retromolar spaceg,m,o,q,r

Complex occlusal surfacesa,n,p

Mid-trigonid crest more frequenta,f

Inwardly sloping centroconids and centroconesn

Extra fissures, ridges and lingual crestsa

Larger crown baseh

40 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

linkage disequilibrium (e.g. Hammer et al., 2011) to infer admix- ture with ancient populations. We now have a much more broadly based view of our genetic ancestry; Mendez et al.’s (2012) study shows that the derived STAT2 haplotype, a potential candidate of introgression, was ten times more likely to be found in Papua New Guineans than in other groups, Wall et al. (2013) argue that Neanderthal genes are more prevalent in East Asians than Europe- ans, while Hammer et al. (2011) believe that their genetic analysis is indicative of introgression with a previously unknown transi- tional hominid from Central Africa. In addition to these geographic regions, we now have potential evidence of secondary introgres- sion (i.e. from an AMH population carrying introgressed genes) in North Africa (Sánchez-Quinto et al., 2012) and East Africa (Wall et al., 2013). A new interpretation is that our African ancestry was mosaic in nature, with potentially multiple as yet un-defined hominins contributing to our modern genome (Hammer et al., 2011; Stringer, 2012). Comparisons can be drawn with the idea of population subdivision, as these hominins may represent the beginnings of subspecies division, while being insufficiently differ- entiated to warrant full species status.

The assumption that divergent haplotypes or specific patterns of linkage disequilibrium are indicative of introgression needs to be validated. Such signals could arise from other processes such as fixation of genes or incomplete lineage sorting (Alves et al.,

Table 5 (continued)

Location Trait

Large root canalsh,r

Longer rootsh

Enlarged pulp chambers (‘taurodontism’)a,f,h

Mandibular P4

Strong, continuous transverse cresta,b

Well-developed, medially placed metaconida

Truncated mesiolinguallobea,b

Narrow lingual crownb

Asymmetrical crown shapea,b

Postcranial Trunk Large dorsal sulcus on scapulaem

Long scapulaen

Expanded rotator cuff attachmentsn

Well-marked muscle attachments alongs capulaer

Long, narrow glenoid fossaen

Long clavicles with flattened shaftsn,q,r

Flaring iliac bladesn

Ribcage is narrow at top and flares out and downn

Broad ribcageq,r

Mobile vertebral column set against inferiorly placed sacrumn

Reduced vertical length of the waistn

Limbs Pronounced radial curvaturem

Thick corticesn

Restricted medullary cavitiesn

Expanded articular surfacesn

Robust limb bonesq,r

Well-developed muscle attachmentsr

Short distal extremities resulting in low brachial and crural indicesq,r

Bowing of femorar

Low humeral torsion angles Narrow humeral deltoid tuberositiesc

Robust humeral diaphysisc

Large, transversally humeral headsc

Enlarged epiphyses with large articular surfacesc

Large olecranon fossaec,s

Humeral medial and lateral pillars that are distodorsally smalls

Hands and feet

Flattened first carpometacarpal jointm,r

Elongated polluxm

Long pollical distal phalanxr

Large carpal tunnelsn

Expanded pollical and ulnar distal phalangeal tuberositiesn

Accentuated muscle attachment areasn

Robusticityr

Pelvis Wide pelvisr

Long, plate-like superior pubic ramusi,m,n,r

Anteriorly placed sacrumr

Anteriorly placed pelvic inleti

Triangular shaped ishiopubic regioni

Obtuse subpubic anglei

Internal obturator groove encroaches upon ischial tuberosityi

a Bailey (2002). b Bailey and Lynch (2005). c Churchill and Smith (2000). d Harvati (2003). e Harvati et al. (2007). f Hershkovitz et al. (2011). g Holliday (2003). h Kupczik and Hublin (2010). i Rak (1990). j Santa Luca (1978). k Schwartz and Tattersall (1996). l Spoor et al. (2003).

m Tattersall (1992). n Tattersall (2007). o Tattersall and Schwartz (1998). p Tattersall and Schwartz (2006). q Wood and Lonergan (2008). r Wood and Richmond (2000). s Yokley and Churchill (2006).

S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50 41

2012), and do not exclude the possibility of ancestry. The use of chimpanzee DNA as an ancestral comparison merely shows that the derived states could have evolved any time after the diver- gence with our common ancestor (Lowery et al., 2013). A recent study has demonstrated the plausibility of genetic drift and demic diffusion in creating a cline of introgression from Europe to Asia, which could otherwise be interpreted as differing levels of hybrid- isation (Lowery et al., 2013). It is doubtful that we will be able to overcome the inherent assumptions of modern genetic studies without the retrieval of DNA from specimens ancestral to both Neanderthals and AMH. With luck this could be possible, given the successful retrieval of DNA of a cave bear (Ursus deningeri) from Sima de los Huesos, dated to �400 ka (Valdiosera et al., 2006; Dabney et al., 2013), but future research would be constrained by the decreasing size of DNA fragments which can be retrieved as the age of the specimen increases (Valdiosera et al., 2006).

In addition to the Neanderthal draft genome, we now have genetic evidence from the phalanx found in Denisova cave, dating to �40 ka (Krause et al., 2010). It has been suggested that this spec- imen represents a sister group to the Neanderthals, splitting off around 465 ka (Krause et al., 2010). Original analysis of recovered nuclear DNA suggested introgression with Melanesians at a level of approximately 4.5%, which is presumed to have taken place after the admixture event between Neanderthals and AMH (Reich et al., 2010). A recent study was able to produce a high coverage sequence from the same specimen (Meyer et al., 2012), a finding which has clear implications for the future of the hybridisation debate. With evidence of such a complicated genetic history of our species, most probably fraught with extensive reticulation over a significant period of time, it is clear that the question of Neander- thal–AMH hybridisation is far more intricate than previously anticipated.

Models of admixture

Some have attempted to model the levels of admixture that could result in such seemingly contradictory evidence between mtDNA and nuclear DNA. For instance, Currat and Excoffier (2004) concluded a maximum estimate of 34–120 admixture events in the entire 12.5 ka estimated period of admixture, corre- sponding with a maximum level of introgression of Neanderthal genes at 0.02–0.09%. This estimate does not match the results of Green et al. (2010), although a later Neolithic expansion of H. sapi- ens could have led to a decrease in the existing signal, as could dilution effects and genetic drift (Currat and Excoffier, 2004). A later model estimated interbreeding success rates to be below 2%, which would result in low levels of introgression in mtDNA evi- dence (Currat and Excoffier, 2011). This would predict the disparity between the mtDNA and nuclear DNA evidence, but is dependent on the accuracy of the estimates of the period of admixture.

Another relevant model is that of Belle et al. (2009), who used coalescent theory to compare Neanderthal, AMH and modern human information with simulated genealogies. This work resulted in a best estimate of no admixture between Upper Palae- olithic populations, with a maximum level of 0.001% interbreeding per generation. There are thus obvious incongruities in the predic- tions of different models which could negate their efficacy in this debate. For instance Hawks and Wolpoff (2006) found that the null hypothesis of no introgression could not be rejected, but that the variation found was within the expected range for a subpopulation connected by gene flow, thus refuting the assignation of Neander- thals to a separate species.

A recent model developed by Eriksson and Manica (2012) explored the effect of ancient population substructure. Their model fitted the genetic results more closely than Green et al.’s proposal, again showing that we cannot accept the conclusion of hybridisation

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) Mladeč 25c No introgression Serre et al. (2004) Mladeč 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)

Table 7 Some of the molecular divergence estimates for Neanderthals and AMH.

Divergence estimate (Kya)

Calibration: homo–chimp split (Mya)

References Type of DNA used

407 6–7 Endicott et al. (2010) mtDNA 435 6.5–7.5 Endicott et al. (2010) mtDNA 465 (317–741) 4–5 Krings et al. (1999) mtDNA 461–825 4.7–8.4 Green et al. (2006) mtDNA 516 (465–569) 6.5 Green et al. (2006) nDNA 550–690 4–5 Krings et al. (2006) mtDNA 631–789 4–5 Beerli and Edwards

(2002) mtDNA

660 (520–800) 6–8 Green et al. (2008) mtDNA 825 6.5 Green et al. (2010) nDNA and

mtDNA

42 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

until we have ruled out other phenomena. However, a major prob- lem arises in the dependence of models such as this on estimates of the time period of hybridisation. The timing has a significant effect on expected levels and direction of introgression (Currat and Excoffier, 2011). Speciation is not instantaneous, often taking 2– 4 ma to reach full behavioural, ecological or reproductive isolation. Therefore, the probability of reticulation should increase as we approach the point of cladogenesis.

Estimates of the time of the Neanderthal–AMH divergence, sum- marised in Table 7, cover a wide range of 407–825 kya. Comparably, Endicott et al. (2010) dated the population divergence (as opposed to the genetic divergence) of the two to 343–373 kya. The calibra- tion point of the human–chimpanzee divergence is the main con- tributor to the wide range seen in Table 6, as this could date anywhere between 6 and 11 ma (Patterson et al., 2006; Jensen- 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 the Orang-utans from African Apes (�23–13 Mya) (Holmes et al., 1989; Patterson et al., 2006). Consequently, the human–chimpan- zee split is not well-suited for use as a calibration point (Endicott and Ho, 2008), and more accurate results could be obtained by the use of multiple internal archaeological or biogeographic calibra- tion points within the Homo lineage (Pulquério and Nichols, 2007; Endicott and Ho, 2008). Methods applying recent estimates of sub- stitution rates could question the use of fossil calibration, with obtained dates being considerably older than those from fossil cal- ibration studies (Fu et al., 2013). Until we can gain more reliable estimates for the divergence time of Neanderthals and AMH that are not accompanied by extremely wide, compounded error mar- gins, assessment of the time of hybridisation and its significance will remain very difficult.

Although it is now widely accepted that non-African humans inherit around 1–3% of their genomes from Neanderthal ancestors (e.g. Green et al., 2010; Prufer et al., 2014; Vernot and Akey, 2014),

there continues to be considerable debate as to when this element was introduced. When publishing the draft Neanderthal genome sequence, Green et al. (2010) admitted the possibility that this apparent introgression could in fact be due to ancestral population structure (see also Eriksson and Manica, 2012). The population structure argument explains the fact that non-Africans share more genetic material with Neanderthals than do sub-Saharan Africans by postulating an ancestral geographical division between sub- Saharan and North-eastern Africans. If this division predated the departure of Neanderthal ancestors from North-eastern Africa, and persisted at least until the first migrations of H. sapiens out of East Africa, then it could account for the genetic affinities of non-African populations and Neanderthals without the need to posit subsequent interbreeding (see e.g. Sankararaman et al., 2012). However, a number of recent studies have cast doubt on the population structure argument, arguing that the sharing of alleles is due at least partially to recent admixture (Prufer et al., 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 beyond these tentative conclusions, arguing that some inbreeding occurred between H. sapiens and Neanderthals more recently than 86 ka. The idea of minor gene flow events between as many as four hominin groups in the Late Pleistocene (H. sapiens, H. neanderthal- ensis, Denisovans, and a fourth, as yet unnamed group (Prufer et al., 2014)) is consistent with current data; however, such data remain insufficient to cast doubt on the integrity of H. neanderthalensis as a species, particularly whilst the extent of allele sharing that is due to ancestral population structure remains unknown.

DNA analyses and their status

There are clear discrepancies between the different sets of genetic evidence, which could be partly explained by complicated demographic and genetic processes in the evolutionary history of the two groups mainly in question. It has been stated that it would be impossible to disprove interbreeding from absence of evidence of introgressed genes, as this absence could also result from low levels of interbreeding (Wall, 2000; Pääbo, 2003; Ghirotto et al., 2011). Therefore the existence of some evidence of admixture is noteworthy, even in the form of low levels of introgression. While the low rates could be explained by possible pre-zygotic preventa- tive mechanisms to interbreeding (Currat and Excoffier, 2011), Templeton (2005) has commented that levels of gene flow are bio- logically significant if the migration rate multiplied by population size is greater than 1, implying that Green et al.’s (2010) prediction of 1.3–2.7% gene flow would be significant regardless of population size.

Fig. 2. Assumptions underlying use of genetics in taxonomic classification (Ferguson, 2002: 510).

Discussion

After reviewing the evidence it is necessary to return to previ- ous models of the speciation process. It would seem that the rela- tionship between Neanderthals and AMH would best be categorised as Mayr’s third stage of allopatry (Mayr et al., 1953): occasional hybrids without free interbreeding, thus resulting in the conclusion that the two populations are each full species. This is the most conservative conclusion, given the sparse evidence for hybrids in the archaeological record, with none of the supposed hybrids showing any necessary criteria except intermediate char- acteristics, which are expected to appear long after the predicted periods of interbreeding. The position is complicated further by the difficulty of identifying hybrids in the fossil record, as soft-tis- sue characteristics may be needed (Jolly, 2001). Nevertheless, even if hybridisation did occur, both groups maintained distinct mor- 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 the Neanderthals evolutionary lifespan. Whereas Green et al.

(2010) argue for interbreeding at an earlier stage (>60 ka), Currat and Excoffier (2011) have aimed to explain the data in terms of more recent contacts in Europe. While this debate remains unre- solved, we cannot make general conclusions regarding the signifi- cance of the interbreeding, but it remains clear that it was not sufficient to affect Neanderthal’s species status.

The use of genetic evidence to decide taxonomic status relates most comfortably to the Biological Species Concept (BSC). The logic behind this has been demonstrated by Ferguson (2002) (see Fig. 2), 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 and behavioural evidence (Ferguson, 2002), which may be more difficult to access. Problems also arise from the previously men- tioned misapplication of the criterion of reproductive isolation, and the fact that relatively few genetic changes may be required for reproductive isolation through pre-zygotic (e.g. behavioural, ecological, physical) isolating mechanisms (Ferguson, 2002), which are the main candidate for the barrier limiting interbreeding between Neanderthals and AMH (Klein, 2008). Such mechanisms could include sociocultural differences (Holliday, 2006), social avoidance or assortative mating (Barton and Riel-Salvatore, 2012) and low survival of hybrids (Currat and Excoffier, 2011; Ghirotto et al., 2011). All of these are more porous than true post-zygotic isolating mechanisms (reproductive isolation caused by genetic differences) (Garrigan and Kingan, 2007), meaning that limited introgression, as evidenced by genetic studies, could occur under such a model.

The discrepancies between recent nuclear studies and previous mitochondrial evidence can be explained by demographic and genetic processes such as genetic swamping (Garrigan and Kingan, 2007) following the probable later migration of Neolithic populations, or neutral genetic drift (Serre and Pääbo, 2006), which could erase mitochondrial signals of low levels of introgression. If Green et al.’s (2010) estimates of interbreeding are correct, they would have to be considered biologically significant (Templeton, 2005), however the results have to be replicated with a much lar- ger sample base. The disparity between genetic and morphological evidence could be allowed despite some hybridisation, as under a model of introgression of adaptive alleles from rare interbreeding events, such alleles will probably be unrelated to morphology (Hawks et al., 2008). While genetic evidence fulfils some of the cri- teria for species identification, such as genotypic clusters which would construe species status to both groups under the Genotypic Cluster Species Concept (Mallet, 2007), it cannot prove genetic exclusivity as of yet. Nevertheless, the low estimates of interbreed- ing can be accepted under the original BSC. If we accept the genetic

44 S. White et al. / Journal of Anthropological Archaeology 35 (2014) 32–50

evidence, including the contribution of supposed transitional hom- inins in Africa and the Denisovan sister-group, we would have to conclude that the speciation of H. sapiens was a long process with potentially frequent interbreeding events.

The particular replacement pattern seen in Europe of AMH spreading and eventually replacing the indigenous Neanderthal population is of interest. Dobzhansky (1944) was the first to com- ment that this pattern matched that of one species replacing the other. Neves and Serva (2011) came to a similar conclusion, how- ever with the more conservative statement that the extinction of one subpopulation was expected under such long-term coexis- tence. This would present a problem under the Ecological Species Concept of Van Valen (1976), as such a pattern would only result from ecological competition and cohabitation of similar niches (Garrigan and Kingan, 2007). This model could allow for some adaptive hybridisation, with the expanding population acquiring advantageous genes from the indigenous population (Garrigan and Kingan, 2007), yet extinction by higher levels of hybridisation is impossible as the two groups did not merge into one taxon.

Morphological analysis leads to a more certain conclusion. The existence of two separate morphospecies, with Neanderthals being more defined and easily differentiated by a list of traits, would ful- fil the requirements of the Phylogenetic Species Concept of Nixon and Wheeler (1990), as well as traditional taxonomy and cladistics, where theoretically one autapomorphy is sufficient to define a spe- cies (Simpson, 1951). It could also support species status under the Recognition Concept of Paterson (1981), as the large morphological differentiation would debatably have resulted in different species- specific mate recognition systems (SMRS) (Tattersall and Schwartz, 2006). The extinction of Neanderthals, potentially as late as 28 kya (Finlayson et al., 2006; Hawks et al., 2008), would argue for sepa- rate evolutionary fates, and thus support species status under the Evolutionary Species Concept of Simpson (1951).

Conclusion

The aim of this synthesis was to assess the validity of the assumption that interbreeding between Neanderthals and AMH, as suggested by Green et al. (2010) among others, would require that the two be subsumed into H. sapiens. This assessment is dependent on proper understanding of the speciation process 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 conclusion, with the two groups fulfilling all criteria. The only counterargument involves a recent misinterpretation of the Biolog- ical Species Concept as requiring absolute genetic and reproductive isolation. This is understandable, but adherence to this strict crite-

rion would result in a gross overestimation of the number of spe- cies, especially in plant taxonomy but also in mammals, as members of different genera and families regularly interbreed without losing their cohesion as separate species. Considering the time periods required for full speciation and the relatively short lifespan of the Neanderthals, interbreeding should be expected but is nonetheless irrelevant to their species status.

While genetic evidence seems to indicate some introgression of Neanderthal and other hominin genes into the modern human genome, these results require wider replication, as well as further research into the ancestral genome before speciation occurred. Morphological assessment provides little convincing evidence for the existence of hybrids, yet it may be more reliable to assume that Neanderthals and AMH interbred, and thus that late Homo species formed a syngameon. While molecular clocks have not progressed far enough to discover when introgression occurred relative to the point of genetic divergence, it is clear that these two populations reached a sufficient stage of the speciation process that any inter- breeding between them did not result in the merging of the taxa. The extinction of the Neanderthal lineage was not caused by hybridisation, with Neanderthals and AMH maintaining their own evolutionary fate despite limited interbreeding.

The question has to be raised ‘‘Why is the species debate still so prominent in the field of palaeoanthropology?’’. Gould’s (1991) commentary on the races debate has some relevance here, as he has argued that such disputes do not further the study of variation between groups, and hinder the search for causal relationships between this variation and external influences. Considering this position, it could be argued that while the species debate remains pertinent to issues of systematic classification and phylogenetics, its resolution will not contribute to our understanding of the bio- logical relationship between AMH and Neanderthals, as interbreed- ing cannot have had the significant effect required to alter Neanderthal species status. The only conclusion that can be reached, regardless of further genetic evidence, is that Neanderthals and AMH constitute separate species in every meaning of the term. The knowledge that full biological speciation can occur in Homo in the space of half a million years, despite significant periods of cul- tural and geographic overlap between the groups, has wide impli- cations. While some cultural behaviours may have permeated this boundary, this did not prevent speciation from taking place.

Acknowledgments

We would like to thank three anonymous Journal of Anthropo- logical Archaeology reviewers for their comments on earlier drafts of the manuscript.

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

Concept

Proponent/s

Definition

Advantages

Disadvantages

Biological

Mayr (1964), Dobzhansky (1935)

– ‘‘Species are groups of interbreeding natural populations that are reproductively isolated from other such group’’ (Mayr, 1996: 264)Use morphological divergence as indication of degree of reproductive isola- tion (Mayr, 1996)

– Defines in terms of evolutionary causes of species (Ghiselin, 1974)) – Proposes a criterion for recognition (reproductive isolation)

– Does not apply to asexual organisms (Mayr, 1996)) – Cannot be applied to fossil record (Tattersall, 1992; Boggs, 2001)) – Must be applied inferen- tially through morphological analysis (Foley, 1991; Kimbel, 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 and Ashlock, 1991)) – Species are natural entities (Balakrishnan, 2005)) – Criterion: reproductive iso- lation (Balakrishnan, 2005)

– Cannot apply to allopatric populations (Tattersall, 1992; Quicke, 1993; Boggs, 2001)) – Based on assumptions of evolutionary process, but ob- 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 (Mayr, 1996) – Stresses ecological and reproductive cohesion as maintaining species unity (Mallet, 2007) – Potential for phenotypic cohesion through intrinsic cohesion mechanisms (Harrison, 1998)

– Combines multiple concepts (Mallet, 2007)

– Does not distinguish between internal and external barriers to gene flow (Mayr, 1996) – Claims to be applicable to asexual taxa, when is not (Mayr, 1996) – Characterises evolutionary lineage without indicating how to delineate (Mayr, 1996) – Does not explain how to deal with polytypic species (Mayr, 1996)

Ecological

Van Valen (1976)

– ‘‘Lineage which occupies an adaptive zone minimally different from that of any other lineage in its range and which evolves separately 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)

– Does not apply to all cases e.g. Cichlids (Mayr, 1996) – Numerous cases of sympat- ric species occupying the same niche (Mayr, 1996)

Evolutionary

Simpson (1951), Wiley (1978)

– ‘‘Phyletic lineage (ancestral- descendent sequence of interbreeding populations) evolving independently of others, with its own separate – and unitary evolutionary role and tendencies’’ (Simpson, 1951: 289) – ‘‘Ancestor-dependent pop- ulations maintaining its identity from other lineages and which has its own evo- lutionary tendencies and fate’’ (Wiley, 1978: 18) – From recognition of inter- breeding between species (Boggs, 2001)

– Operational ‘recipe’ for demarcation of fossil species (Mayr, 1996) – Acknowledges that species can maintain morphological and ecological distinctness despite genetic introgression (Boggs, 2001) – Includes lineages effectively separated from ancestral lineage that have not yet acquired reproductive isola- tion (Miller, 2001) – Acknowledges temporal dimension of species (Mayr and Ashlock, 1991)

– Undefined, vague terms (Mayr, 1996) – Only applicable to mono- typic species (Mayr, 1996; Boggs, 2001) – No empirical criteria to test (Mayr, 1996) – Does not help in case of chronospecies (Mayr, 1996) – Requires knowledge of evolutionary history (Boggs, 2001) – Do not know historical fate of extant lineages (Quicke, 1993) – Defines phyletic lineage, not 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

cluster

Mallet (1995, 2007)

– ‘‘Separate species are

recognised if there are several clusters separated by multilocus phenotypic or genotypic gaps. A single species . . . is recognised if there is only a single cluster in the frequency distribution of multilocus phenotypes and genotypes’’ (Mallet, 2007: 11)

– Practical application of the Biological Species Concept (Mallet, 2007) – Avoids tautological argu- ment (Mallet, 2007) – Can identify majority of genotypic clusters morpho- logically (Mallet, 2007) – Includes polytypic species (Mallet, 1995) – Incorporates genetic and morphological indications of species (Mallet, 1995)

– Can be affected by (Mallet, 1995): – Sex-linked genes – Chromosomal inversions – Polyploidy – Linkage disequilibrium

Phenetic

‘‘Pheneticists’’(1960– 70s)

– Defined in numerical or statistical terms (Mallet, 2007)

– Similar to those already used by taxonomists (Mallet, 2007) – Practical and applicable to all cases (Balakrishnan, 2005)

– Treats species as classes defined by traits of organisms, not as individuals with properties necessary for species category (Ghiselin, 1974) – Classifies by degree of resemblance, ignoring evolu- tionary theory (Ghiselin, 1974)

Phylogenetic (multiple)

Cracraft (1983, 1987), Hennig (1966); Nixon and Wheeler (1990), Baum and Donoghue (1995)

– ‘‘The smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent’’ (Cracraft, 1983; 170) – Revival of purely morpho- logical concept (Mayr, 1996) – Morphology taken to rep- resent reproductive cohesive- ness (Tattersall, 1992) – Species have fundamental roles for systematics and evolutionary theory (Tattersall, 1992) – Character-based (e.g. Nixon and Wheeler) and History/ Lineage-based (e.g. Hennig, 1966; Baum and Donoghue, 1995) (Balakrishnan, 2005)

– Taxonomic units as units of evolution, therefore applicable both to evolutionary theory and systematics (Tattersall, 1992; Kimbel, 1991) – Meets the requirements of phylogenetic theory while avoiding dependence on pro- cesses (Nixon and Wheeler, 1990) – Acknowledges process of speciation, and that infraspe- cific taxa may be incipient species (Nixon and Wheeler, 1990) – Integration of theoretical and operational viewpoints (Kimbel and Rak, 1993) – Consistent with nature of species as individuals (Kimbel, 1991)

– Ignores subspecies categories, so inapplicable to polytypic species (Tattersall, 1992; Baum and Donoghue, 1995) – Imprecise – different ap- proaches used to the defini- tion of characters (Nixon and Wheeler, 1990) – Could overestimate number of species (Quicke, 1993) – Must reject character-based concepts as definitions ignore evolutionary process (Baum and Donoghue, 1995) – Tautological: uses phylog- eny to determine species which are then used to esti- mate the phylogeny (Mallet, 1995) – Ignores Mendelian and population genetics (Avise and Wollenberg, 1997) – Difficult to determine true fixation (Balakrishnan, 2005)

Recognition

Paterson (1981)

– Species boundaries are delimited by the shared specific-mate recognition system (SMRS) (Paterson, 1981) – Dependent on genealogical role of species (Tattersall, 1992) – Most inclusive population of individual, bi-parental organisms that share a com- mon fertilisation system,

– Acknowledges problems of Biological Species Concept and tries to incorporate solutions to these (Tattersall, 1992)

– Same problems as found with Biological Species Concept (Boggs, 2001) – SMRS are generally exter- nal, and therefore hard to recognise in the fossil record (Tattersall, 1992) – Difficulty in application to humans and primates in gen- eral, and therefore to the fos- sil record (Kimbel, 1991; Jolly, 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 (Harrison, 1998)

– Can only diagnose species by tautology (Jolly, 1993) – May underestimate number of species (Kimbel, 1991)

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