http://informahealthcare.com/ahbISSN: 0301-4460 (print), 1464-5033 (electronic)

Ann Hum Biol, 2014; 41(4): 312–322! 2014 Informa UK Ltd. DOI: 10.3109/03014460.2014.922616

REVIEW

Diagnosing Homo sapiens in the fossil record

Christopher Brian Stringer1 and Laura Tabitha Buck1,2

1Natural History Museum, Cromwell Road, London, UK and 2University of Roehampton, Whitelands College, Holybourne Avenue, London, UK

Abstract

Background: Diagnosing Homo sapiens is a critical question in the study of human evolution.Although what constitutes living members of our own species is straightforward, in the fossilrecord this is still a matter of much debate. The issue is complicated by questions of speciesdiagnoses and ideas about the mode by which a new species is born, by the argumentssurrounding the behavioural and cognitive separateness of the species, by the increasingappreciation of variation in the early African H. sapiens record and by new DNA evidence ofhybridization with extinct species.Methods and results: This study synthesizes thinking on the fossils, archaeology and underlyingevolutionary models of the last several decades with recent DNA results from both H. sapiensand fossil species.Conclusion: It is concluded that, although it may not be possible or even desirable to cleanlypartition out a homogenous morphological description of recent H. sapiens in the fossil record,there are key, distinguishing morphological traits in the cranium, dentition and pelvis that canbe usefully employed to diagnose the H. sapiens lineage. Increasing advances in retrieving andunderstanding relevant genetic data provide a complementary and perhaps potentially evenmore fruitful means of characterizing the differences between H. sapiens and its close relatives.

Keywords

Fossil record, hybridization, Neanderthal DNA,species definition

History

Received 30 April 2014Accepted 1 May 2014Published online 16 June 2014

Diagnosing Homo sapiens

It is self-evident that diagnosing Homo sapiens is a funda-

mental question in human origins. For most taxa, any

specimen in question can be compared to the type in order

to assess the case for its inclusion within that species. Yet, as

so often, our own species is seen as somewhat of a special

case. The type specimen for H. sapiens is Linneaus himself

(Notton & Stringer, 2010; Stearn, 1959); however, this is

more of a ceremonial honour than a useful taxonomic aid.

Being the only remaining representatives of our genus, all

living humans are similar enough, with demonstrable inter-

fertility, that there is no question as to which species they

belong. Diagnosing H. sapiens has only been regarded as an

issue of importance since other hominin species were found

and acknowledged, beginning with the discovery of the

skeleton from the Neander Valley in 1856, which was

subsequently named as the holotype of H. neanderthalensis

in 1864 (King, 1864). For many extinct hominins their species

definition is far from clear and, in diagnosing other species,

we must simultaneously diagnose our own. The delineation

of H. sapiens has varied widely since the discovery of fossil

human species and, although there are areas of agreement for

many, there is no overall consensus on what constitutes

H. sapiens. In recent years this question has been complicated

further by the genetic evidence, which shows that Pleistocene

species may have interbred with relative frequency, although

not necessarily with high levels of compatibility.

Underlying evolutionary model

Historically, different diagnoses of H. sapiens have been

influenced by their underlying evolutionary model. For many

years there has been disagreement about the mode by which

H. sapiens originated and came to populate the world and

about the explanation for the geographic differences in

phenotype seen in people from different regions today (see

for example Stringer (2014) for an overview of contrasting

models). Since the late 1980s, this disagreement has been

popularly distilled into the dichotomy between Recent

African Origin (RAO) and Multi-regionalism. Adherence to

these models leads to very different characterizations of the

species H. sapiens.

The idea of gradual, regional evolution of humans like

ourselves from local archaic populations is associated histor-

ically with Hrdlicka, Weidenreich, Coon and Brace (Stringer,

1994), but in its modern incarnation as Multi-regionalism,

it has largely been promulgated by Wolpoff and colleagues.

Multi-regionalists view all Homo from, and including,

H. erectus as one species (Wolpoff et al., 1994; Wolpoff &

Caspari, 1997a) and, if H. erectus and H. sapiens are

combined, the name H. sapiens has priority (Wolpoff &

Caspari, 1997b). Thus, the Multi-regionalist paradigm pro-

poses a single, polytypic H. sapiens species evolving regional

Correspondence: Laura Tabitha Buck, Natural History Museum,Cromwell Road, London SW7 5BD, UK. Tel: 020 7942 7004. E-mail:l.buck@nhm.ac.uk

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

variations from 41 Ma onwards, with significant gene

flow between regions preventing speciation. In this

view species can only be created by cladogenesis and the

cladogenetic event in this case was the origin of the genus

Homo, however much variation this might require the

resultant species to contain (Wolpoff et al., 1994;

Wolpoff & Caspari, 1997a).

During the last 25 years the model that has usually been

regarded as the antithesis of Multi-regionalism is the Recent

African Origin (RAO) model. As the name suggests, this

model posits that H. sapiens originated in Africa relatively

recently and subsequently spread out to inhabit the rest of the

world, replacing existing archaic populations in each region.

The date of origin of H. sapiens in this model has changed in

the face of new discoveries and dating work. Initially it was

placed at �100 ka, but dates for the appearance of ‘‘anatom-

ically modern humans’’ (that is to say fossils that are

demonstrably closer to living humans in morphology than to

any other species) in the fossil record now lie at �200 ka,

while the origin of the lineage of H. sapiens could be much

further back, at �400 ka (Stringer, 2012a). Although initially

vague in terms of the mode of speciation, at times there has

been an emphasis on punctuationalism, cladogenesis and the

importance of a late bottleneck by some advocates of RAO

(Stringer, 2002).

There have, of course, been many intermediate viewpoints

between these two extremes, which have tended to be

simplified to highlight the contrasts between the models and

their protagonists. Brauer’s (African) Hybridization and

Replacement model, for example, combines RAO with a

degree of regional interbreeding between Africa-derived

H. sapiens and other hominin populations (e.g. Brauer,

1992, 2011), but he advocates a wider diagnosis of the

species, classifying both Middle Pleistocene Africans and

Neanderthals as ‘‘archaic H. sapiens’’. Multi-regionalism in

the strict or classic sense, as described above, has been

modified over the years in response to new data and today,

whilst its advocates would still argue for substantial and

widespread gene flow in the Pleistocene as the major impetus

behind the evolution of H. sapiens, many would admit that

Africa has been the principal source of genetic input.

A formalized version of this viewpoint is Smith and

Trinkaus’ Assimilation model (Smith, 1992; Trinkaus, 2005).

Improvements in dating over the last few decades have

enabled clarification of the chronology of recent human

evolution, showing there was a co-existence or alternation of

H. sapiens and Neanderthals in Israel, disproving the idea that

Neanderthals in Eurasia always preceded H. sapiens

(Grun et al., 2005). Genetic analyses also provided important

support for RAO, by showing that an African origin was the

most parsimonious explanation for the fact that non-African

genetic variation is largely a sub-set of that seen in Africa.

These advances led to a decline in the popularity of Multi-

regionalism and the pre-eminence of RAO models. For the

last two decades, the most popular view of H. sapiens has

been that of an African species that originated during the

Middle Pleistocene and which can be differentiated from

other Pleistocene species such as Neanderthals and H. erectus,

whom they are thought to have replaced on their dispersal out

of Africa.

Recently, however, new genetic data have shown that

extant H. sapiens did not derive purely from an African

origin, demonstrating multi-regional contributions to the

recent human gene pool. There is now evidence for inter-

breeding between both Neanderthals and H. sapiens and

between Denisovans and H. sapiens (see below). Thus, the

importance of a greater degree of genetic input from other

species has had to be accepted by those who favour RAO and

in some quarters there is renewed interest in Multi-regionalist

ideas (Finlayson, 2013; Hawks, 2010; Stringer, 2014).

Likewise, the greater numbers of fossils now available has

sometimes complicated issues of taxonomy rather than

simplified them (e.g. Hublin, 2014; Lordkipanidze et al.,

2013; Spoor, 2013) and we are still far from an agreement on

what constitutes H. sapiens in the past.

A definition of H. sapiens based on recent variation

One of us (CS) found from his doctoral research that certain

cranial angles and indices convincingly separated a group of

recent H. sapiens, Upper Palaeolithic H. sapiens and fossils

such as Skhul and Omo Kibish 1 from Neanderthals and other

‘‘archaic’’ groups (Stringer, 1974) and, thus, became inter-

ested in a morphological diagnosis of Homo sapiens. Using

measurements from Howells’ (1973) database, he formulated

the idea of using the range of recent H. sapiens variation to

diagnose H. sapiens in the fossil record. Fossils that fell

within the range of recent variation could be classed as

H. sapiens, while those that did not, by implication, would not

represent this species. Using Howells’ and his own data,

Stringer (1974, 1978) attempted to encapsulate key H. sapiens

traits such as a domed neurocranium, reduction in facial size

and projection, and increased basicranial flexion. Based on

these characteristics, Day & Stringer (1982) formulated what

they termed a ‘‘working definition’’ for H. sapiens

(Day & Stringer, 1982: 835). The purpose of this was to

test whether the Omo 1 fossil from Ethiopia should be

included in H. sapiens sensu stricto, as Stringer (1974, 1978)

had argued, or in a Neanderthal grade, as asserted by workers

such as Brose & Wolpoff (1971). Omo Kibish in Ethiopia is

key in diagnosing H. sapiens in the fossil record, as it is one of

the earliest known H. sapiens sites. It is also intriguing

because of the degree of morphological disparity between two

crania found there, Omo 1 and Omo 2. Omo 1 was found

partially in situ and in association with extinct fauna, whereas

Omo 2 was a surface find from �2.5 km away, thus

the relationship between the two specimens is unclear

(Day & Stringer 1982). Despite the lack of context for Omo

2, both specimens have been argued to date from �195 ka

(Shea et al., 2007), with this age for Omo 1 supported

by direct uranium series dating (Aubert et al., 2012).

However, there are many differences between the two crania

in features such as neurocranial globularity and occipital

morphology.

To see if Omo 1 could be included in H. sapiens sensu

stricto, Day and Stringer formulated a list of criteria for the

species based on the presence of putative shared H. sapiens

characteristics. The authors noted that the features used to

define H. sapiens sensu stricto would not be found in all

extant specimens, but suggested that the majority should be

DOI: 10.3109/03014460.2014.922616 Diagnosing Homo sapiens in the fossil record 313

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

present. In addition, they acknowledged that some of the

features might also be found in non-H. sapiens fossils. They

suggested that a fossil should have over 50% of the diagnostic

features to be classed as H. sapiens. Based on this list it was

concluded that Omo 1 was H. sapiens sensu stricto, while

Omo 2 was not. In fact, in some aspects of morphology, the

latter fossil more closely resembled H. erectus than H.

neanderthalensis or H. sapiens (Day & Stringer, 1982). The

criteria chosen in the paper were deliberately strict in order to

be conservative regarding the inclusion of the fossil Omo

specimens in H. sapiens. They were never intended for the

diagnosis of large samples of recent H. sapiens based on

single traits, since it was recognized that not all recent

humans would display all of the characteristics.

The provisional 1982 criteria were subsequently modified

in recognition of their under-estimation of the amount of

variation in the species (Day & Stringer, 1991; Stringer et al.,

1984), but when the original criteria were tested by other

researchers on populations of recent H. sapiens, some of the

characteristics were found to be problematic (Lahr, 1996;

Lieberman et al., 2002; Wolpoff, 1986). Lahr (1996) found

that some recent populations fell outside the ‘‘modern’’ range,

as defined by Day & Stringer (1982) for some criteria, and

she concluded that this showed this diagnosis of H. sapiens

was insufficiently broad. In particular, she found the required

frontal angle for inclusion in H. sapiens was defined too

narrowly with, for example, her Fuegian/Patagonian sample

mean falling outside the range given by Day and Stringer

(Lahr, 1996). Wolpoff (1986) also found that several

Australian fossil crania did not meet the criteria, although

there was no question that they were H. sapiens. He wrongly

suggested that there was a Euro/African bias in the definition,

but this was refuted by Lahr (1996), who found the

problematic criteria were spread among different populations,

including Europeans.

A more comprehensive fossil record also began to show

glimpses of the much greater variation that had existed even

in the recent past. This included fossils such as Kow Swamp,

Willandra Lakes and Coobol Crossing from Australia and

Kennewick Man from North America. Only a sub-sample of

this variation continues in the present day, perhaps due to

population extinction events and homogenization within

Homo sapiens during the last 15 000 years. The need to

include earlier variation in any diagnosis of H. sapiens was

clear. Stringer’s subsequent phenetic analyses showed how it

was possible to look at differences between fossils as a whole,

rather than at individual characters and to see that, following

their divergence from the last common ancestor (LCA),

Neanderthals and H. sapiens had changed in different ways,

with globularization of the neurocranium and reduction in

face size predominating on the H. sapiens lineage and an

increase in neurocranial size and a change in facial shape

(with an increase in mid-facial prognathism) predominating

on that of the Neanderthals (Stringer, 1978, 1994).

Schemes such as that of Day & Stringer (1982) used all

the chosen criteria with equal weighting in their comparisons

of different taxa, but the expression of some traits may be

due to homoplasy or plasticity, and some are clearly

correlated with each other. Cladistics teaches us that only

synapomorphies (shared, derived characteristics), identified

with reference to one or more outgroups, should properly be

used to define relationships. An organism’s skeleton is able

to adapt to its environment during its lifetime due to

remodelling in response to strain and some regions are more

plastic than others, depending on levels of canalization

(Buck et al., 2010); thus some skeletal traits should be

treated with caution. The phylogenetic utility of a plastic

region should not be discounted out of hand, however. Von

Cramon-Taubadel (2009) has shown that masticatory regions

of the cranium are more plastic than non-masticatory

regions, as would be expected, but they are nonetheless no

less effective at reconstructing human population history.

It may also be profitable to consider the ontogeny of

different features. A mental eminence, or chin, is present (in

variable form) in Neanderthal and Paranthropus boisei

fossils (Schwartz & Tattersall, 2000; Wolpoff, 1986).

However, it is not seen in juveniles, whereas a chin is

always present in H. sapiens from an early age (Schwartz &

Tattersall, 2000). Not all traits are equally informative;

therefore, this is something that should be taken into account

in building species diagnoses.

Branches or tips?

Even if it is agreed, based on RAO, that H. sapiens is a recent

species, distinct from Neanderthals and from the probable

LCA, H. heidelbergensis, at what point do we define the cut-

off for H. sapiens? Should only the tips of the phylogenetic

tree be designated H. sapiens (or indeed H. neanderthalensis);

should the hypodigm contain only those individuals that

display all the traits diagnostic of that species or should there

be a looser definition (see Figure 1)?

One option would be to diagnose H. sapiens by compari-

son with H. neanderthalensis, i.e. to define as belonging to

H. sapiens anything on the H. sapiens lineage after the split

with the LCA of Neanderthals and H. sapiens (e.g. Stringer,

2002). The draw-back of this approach is that there is a great

deal of morphological variation in fossils that most would

agree lie on the H. sapiens lineage, after the split with

H. neanderthalensis. Not only do diagnostic H. sapiens

features not appear all at once, as a complete package, but,

where they appear, they appear in different combinations (see

below). This being the case, the question is what to do with

specimens that fall between the LCA and those specimens

that have the full suite of H. sapiens characteristics. The term

‘‘archaic H. sapiens’’ has been something of a conceptual

dustbin, often being used for specimens alternatively referred

to H. heidelbergensis or H. neanderthalensis, but one of us

(CS) has favoured using it to designate those members of the

H. sapiens lineage that lack a majority of the traits charac-

teristic of the living taxon. This term is then often juxtaposed

with the term ‘‘modern’’ H. sapiens. However, this is

potentially confusing due to the semantic baggage of the

word ‘‘modern’’, which may also imply behavioural/cognitive

criteria as well as morphological ones. Although this

difficulty may be avoided by the popular term ‘‘anatomically

modern’’ H. sapiens, this term can also carry its own baggage

with the implication that ‘‘modern’’ H. sapiens are somehow

an improvement on past populations and that evolution is

progressive.

314 C. B. Stringer & L. T. Buck Ann Hum Biol, 2014; 41(4): 312–322

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Another option which CS previously favoured (as dis-

cussed above) was to limit the use of H. sapiens to those

specimens that display the full suite of H. sapiens traits and

separate those ‘‘H. sapiens’’ that only show some of the

required traits as a separate species. The same usage could

also be applied to separate ‘‘classic Neanderthals’’ and those

fossils that show some, but not all H. neanderthalensis traits.

If this scheme is followed, the name with priority for the

species intermediate between H. heidelbergensis and

H. sapiens would probably be H. helmei (Stringer, 1996)

[this application of the species named from the Florisbad

cranium is distinct from the subsequent usage by Foley &

Lahr (1997)] and the equivalent designation for specimens

intermediate between H. heidelbergensis and H. neandertha-

lensis would probably be H. steinheimensis (see Figure 1[A]).

Yet to use these distinctions merely atomizes the problem

rather than solving it; unless there is truly punctuational

change, populations diverge by degrees and there will always

be intermediates between any two taxa. In this case it would

be very difficult to separate H. steinheimensis and

H. neanderthalensis based on morphology. Neanderthal

traits seem to appear relatively gradually in the fossil record

with specimens such as Swanscombe, Steinheim and Sima de

los Huesos exhibiting different mosaics of Neanderthal

characteristics (Stringer, 2002), much as early African

H. sapiens display variable H. sapiens characteristics

(see below). Differentiating them from the LCA and from

the terminal taxon therefore becomes rather arbitrary.

To call these indeterminate specimens ‘‘early H. sapiens’’

and ‘‘early H. neanderthalensis’’ is another option (see

Figure 1[B]), which, although it lacks taxonomic precision, is

perhaps most representative of the biological reality. The

conceit of species as a series of totally distinct, homogenous

entities may be helpful when considering fossil phylogeny,

but a series of over-lapping, interbreeding and slowly

diverging populations is closer to what we actually see in

living species (Ackermann, 2010; Jolly, 2001; Kelaita &

Cortes-Ortiz, 2013). The early parts of both the H. sapiens

and H. neanderthalensis lineages show some of the lost

diversity that once existed and both will contain groups not

ultimately ancestral to later members of either species.

If these terms are employed it logically follows to refer

to ‘‘recent’’ or ‘‘late H. sapiens’’ and perhaps also to ‘‘late

H. neanderthalensis’’.

A purely morphological diagnosis?

It has been argued that Homo species are different from other

animal species, that they are a special case because of their

great behavioural flexibility and unique reliance on culture

(e.g. Wolpoff & Caspari, 1997a). Can we only truly define our

species based on a combination of behavioural and morpho-

logical traits? This is a question that has engendered much

debate and which has, to a certain extent (excepting Wolpoff

and Caspari), been split along disciplinary lines, with

palaeoanthropologists and archaeologists both proclaiming

the primacy of their particular area of interest. It is also at the

crux of the previously discussed issue as to whether there is

a distinct difference between recent or ‘‘modern’’ H. sapiens

and the rest of our lineage post-dating the split from the LCA

with H. neanderthalensis.

What constitutes ‘‘H. sapiens behaviour’’ is at least as

nebulous a concept as what constitutes ‘‘H. sapiens anat-

omy’’. Traditional markers of recognizably ‘‘modern’’ H.

sapiens behaviour have been said to include:

Increasing artefact diversity; standardization of artefact

types; blade technology; worked bone and other organic

materials; personal ornaments and ‘art’ or images;

structured living spaces; ritual; economic intensification

reflected in the exploitation of aquatic or other resources

that require specialized technology; enlarged geographic

range; [and] expanded exchange networks (McBrearty &

Brooks, 2000: 491).

The arrival of this complex of behaviours has been termed a

Human Revolution (Mellars & Stringer, 1989) and its

description was initially focused on the beginning of the

European Upper Palaeolithic. In that context and at

that time, the term described the seemingly sudden appear-

ance of these complex behaviours about 35 ka (Mellars &

Stringer, 1989).

Figure 1. (A) H. sapiens andH. neanderthalensis as species representedonly at the tips of the phylogenetic tree, thoseindividuals with all the traits judged to bediagnostic. H. helmei and H. steinheimensisas intermediate species between eachterminal species and last commonancestor (LCA), here suggested to beH. heidelbergensis. (B) Looser definitions ofH. sapiens and H. neanderthalensis includingall populations after the split from the LCA.Both species encompass considerablemorphological variation along their lineagesand populations which go extinct withoutissue. The overall topography of the bothtrees and the estimated divergence and LCA‘‘dates’’ are derived from a study of wholemtDNA genomic data (Stringer 2012c).

DOI: 10.3109/03014460.2014.922616 Diagnosing Homo sapiens in the fossil record 315

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Despite the intuitive appeal of the Revolution idea, the

development of so-called modern behaviour, as with

‘‘modern’’ morphology, actually seems much more piece-

meal. It appears in the fossil record in fits and starts in

different places at different times, not as a package tied to

anatomical ‘‘modernity’’. As such it can be argued that

‘‘modern’’ human behaviour loses its utility as a diagnostic

criterion for the physical species. Indeed, there are strong

arguments against the conflation of behaviour and morph-

ology. At one extreme, for Klein (2000, 2008), the two were

completely decoupled so that ‘‘morphological modernity’’

appeared at least 100 ka before the punctuational appearance

of ‘‘behavioural modernity’’, said to be the result of novel

genetic mutations affecting the brain about 50 ka. Some

aspects of ‘‘modern’’ behaviour, however, certainly seem to

have been present in earlier H. sapiens populations at

�100 ka, for example the shell beads, ochre use and burial

behaviour from Skhul and Qafzeh (Bar-Yosef Mayer et al.,

2009; Salomon et al., 2012; Vanhaeren et al., 2006). In fact,

the early emphasis on Europe seems to have been more a

construct of the history of archaeology than a record of

exceptional behaviour in Europe (McBrearty & Brooks,

2000). As earlier and earlier examples of ‘‘modernity’’

emerged from Africa, this material was incorporated into the

Revolution theory, such that the birth of H. sapiens behaviour

might indeed have been more closely coeval with the birth of

anatomical H. sapiens in Africa at �200 ka (McBrearty &

Stringer, 2007).

Increasingly there is potential evidence for some of the

supposed hallmarks of behavioural ‘‘modernity’’ in other

species, particularly in Neanderthals. These include the use of

pigments (Zilhao et al., 2010); the possible symbolic use of

feathers (Finlayson et al., 2012; Peresani et al., 2011); dietary

breadth and diversification (Stringer et al., 2008); the

generally accepted evidence for intentional burial (e.g.

Rendu et al., 2013); and the much-disputed Chatelperronian

industry (e.g., Bailey et al., 2009; Bar-Yosef & Bordes, 2010;

Higham et al., 2010; Zilhao et al., 2006). Although not all

of these findings are universally accepted as evidence of

complex cognition, taken as a whole, they represent the slow

dissolution of a profound symbolic and technological demar-

cation between the behaviour and cognition of H. sapiens and

H. neanderthalensis (d’Errico & Stringer, 2011). Conversely,

where anatomically ‘‘modern’’ human remains are found,

they are not necessarily found in conjunction with evidence

for the whole ‘‘modern’’ human behavioural package. The

best example of this is in Australia, where as far as we know

only fully ‘‘modern’’ humans have ever lived, but where the

archaeological record apparently lacks consistent signals of

the supposed signature of behavioural ‘‘modernity’’ until well

into the Holocene (Brumm & Moore, 2005; but compare

O’Connell & Allen, 2007).

As Stringer (2002) has noted, using technology as a

taxonomic character is fundamentally ill-advised as it can be

passed between reproductively isolated populations or even

species. Based on the evidence now available, behaviourally

‘‘modern’’ H. sapiens seems too loose a concept to be of

much practical use. In the same way that morphological traits

indicative of H. sapiens are seen to appear (and at times

disappear) piecemeal in the fossil record, such is the case with

the behavioural evidence. Furthermore, some behaviours

argued to be definitively those of H. sapiens are both found

in other species and not found in some indisputably

H. sapiens populations. Although there is clearly a biological

component to behavioural capacity, behaviour in humans is

dominantly a learnt attribute and as such should not be used

to define hominin species. We know from ethnology (for

example, historical hunter-gather groups who lost their

previous abilities to make sea-going boats or fire) that

cognitive and behavioural capacities are not equivalent to

the practice of any given behaviour. Thus, even if there is such

a thing as a distinct human behavioural complex, we cannot

use the archaeological record to definitively prove its absence.

As discussed above, the lack of an absolutely distinct complex

of behavioural and morphological traits that characterizes

‘‘modern’’ H. sapiens makes this without doubt a problematic

concept, which may be made clearer by referring instead to

‘‘recent’’ H. sapiens.

Early H. sapiens in Africa

There is wide variation in fossil humans associated with

Middle Stone Age (MSA) archaeology in Africa, with

material from sites such as Singa (Sudan), Omo Kibish,

Herto (both Ethiopia), Ngaloba (Tanzania), Jebel Irhoud, Dar-

es-Soltane (both Morocco), Eliye Springs, Guomde (both

Kenya) and Florisbad (South Africa), all showing different

combinations of primitive and derived (recent H. sapiens-

like) traits. For some of the more complete specimens a

morphological progression can be suggested between Middle

Pleistocene fossils and recent H. sapiens—for example the

BOU-VP-16/1 cranium from Herto. Although this fossil is

primitive-looking in its occipital shape and the strong

supraorbital tori, it also has derived features not seen in

Mid-Pleistocene African hominins such as Broken Hill and

Bodo. These include a more globular neurocranium and

retracted face, which ally it to H. sapiens (Stringer, 2003;

White et al., 2003). White et al. (2003) concluded that Herto

is morphologically intermediate between more primitive

specimens such as Broken Hill, which they dated to

�500 ka, and more derived specimens from �100 ka, but

they also noted that the Herto material does not represent the

only possible intermediate between H. heidelbergensis and

recent H. sapiens.

A combination of the morphology exhibited by Omo 1 and

2 would provide a different model of H. sapiens evolution

from that suggested by Herto, as exemplified by the ER-3884

cranial material from Guomde, displaying another mix of

primitive and derived characteristics that might plausibly have

led to the morphology of recent H. sapiens. These potential

variations on the H. sapiens theme show that there is unlikely

to be a simple, linear relationship between H. heidelbergensis

morphology and H. sapiens morphology. Alternatively, the

variation between Omo 1 and 2 might reflect the co-existence

of two morphologically distinct populations at that time in

Ethiopia (Stringer, 2002, 2012b). It appears that evolution

progressed separately in different populations, morphological

structure at population level leading to a gradual coalescence

of the full suite of H. sapiens characteristics analogous to

that seen in the genetic data. This has been referred to as

316 C. B. Stringer & L. T. Buck Ann Hum Biol, 2014; 41(4): 312–322

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

an African multi-regionalism, describing the evolution of

regional differences within the continent and between many

inter-fertile sub-divisions of one variable evolving species

(Stringer, 2003, 2012a). The same may have been the case for

Neanderthals in Eurasia too; the gradual but not always

precisely ordered accretion of Neanderthal synapomorphies

can be seen in fossils such as Swanscombe, Steinheim and the

Sima de los Huesos remains (Hublin, 2007).

As discussed above, study of MSA-associated human fossils

shows their great morphological variation, while the available

(if imperfect) chronological control provides only limited sup-

port for the idea of an ordered progression from ‘‘less H.

sapiens’’ to ‘‘more H. sapiens’’ through time. Instead we see

very varied fossils apparently juxtaposed in close temporal

proximity (Stringer, 2012b). Moreover, there is growing

evidence of the survival of early sapiens morphology into the

late Pleistocene at sites like Eyasi (e.g., Brauer, 2011) (see

below), while a key H. heidelbergensis specimen, Broken Hill

1, may well date to the late Middle Pleistocene, within the time

range of the MSA (Stringer, 2012b).

Synthesizing these various developments suggests that the

mechanism for the evolution of H. sapiens traits in different

places at different times could have been repeated population

fluctuations resulting from glacial/inter-glacial and shorter cli-

matic cycles. Such oscillations could have led to the creation/

removal of biogeographical barriers such as the expansion and

contraction of tropical rainforests, or of the Sahara Desert

(Stringer, 2012b). The greening or re-desertification of the

Sahara is likely to have been important for contact between

populations in northern and tropical Africa, facilitating or

preventing expansions. Fluctuations in rainfall would have

similarly created or removed green pathways connecting

populations in tropical and southern Africa (Blome et al.,

2012; Coulthard et al., 2013), whilst also forming barriers of

dense tropical rainforest at times, which were probably

impenetrable to early humans. This would have had direct

demographic effects on human populations, leading to periods

of isolation and even regional extinctions, followed by periods

of dispersal into new habitats or re-occupation of old ones.

The use of refugia into which populations could retreat to

survive the worse of climatic down-turns has been suggested

as a key catalyst of adaptive behavioural changes (Stewart &

Stringer, 2012), but equally it can be argued that climatic

ameliorations were important in fuelling denser, networked

populations, thus facilitating genetic and cultural change

(Stringer, 2012b; Ziegler et al., 2013). The result of these

processes culminated in the composite we call recent

H. sapiens, genetically, morphologically and behaviourally,

but there was never a single centre of origin.

Hybridization in Africa?

It is not only in MSA Africa that the H. sapiens fossil record

is highly variable, complicating interpretations of relation-

ships and species definitions. As mentioned above, there are

also a number of relatively recent African sites with fossils

that exhibit combinations of recent H. sapiens and more

primitive traits, allying them to much older specimens.

Stringer found the Iwo Eleru fossil from Nigeria to be

idiosyncratic in his doctoral research, where it showed

affinities with Ngandong, Saccopastore and Omo 2 (which

are disparate in time, space and inferred taxonomic position),

as well as with recent H. sapiens. This result highlighted the

unusual combination of traits seen in the fossil (Stringer,

1974). It was recently confirmed as dating to the very end of

the Pleistocene (�11.7–16.3 ka) (Harvati et al., 2011);

however, it is morphologically unlike recent African crania

(Harvati et al., 2011, 2013; Stringer, 1974). Despite its late

date, in geometric morphometric comparisons with a wide

range of extant crania, Iwo Eleru falls outside the range of

recent African variation and groups instead with the much

older Elandsfontein and Ngaloba fossils from Africa and with

Skhul and Qafzeh from Israel (Harvati et al., 2011, 2013). The

Ishango fossils from the Democratic Republic of Congo are

slightly older than Iwo Eleru (�20 ka), but, interestingly,

morphometric characteristics and dental size also place them

at the edge of extant African diversity and their inner ear

morphology appears more like that of Middle Palaeolithic

hominins than those of H. sapiens of comparable age

(Crevecoeur et al., 2010). These specimens from Central

and West Africa emphasize how little we know about the

fossil record of large swathes of the continent. They have also

been suggested as evidence of population sub-structure and

the late retention of great morphological diversity in

our species, possibly as a result of hybridization between

H. sapiens and an archaic hominin species, perhaps

H. heidelbergensis (Hammer et al., 2011; Harvati et al.,

2011; Stringer, 2012a,b,c).

Hammer and colleagues’ work on recent African nuclear

DNA shows traces of recent (550 ka) archaic introgression in

Africa from a population that split from the ancestors of

recent H. sapiens at �700 ka (Hammer et al., 2011). They

suggest at least one introgression event could have taken place

in Central Africa [see also Lachance et al. (2012)]. Ishango

notwithstanding, there is virtually no fossil record from this

region, so it is difficult to even speculate about the source of

this introgression. There is also new evidence of an ancient Y

chromosome lineage in West Africa, increasing the estimated

coalescence date for the Y chromosome in H. sapiens to 237–

581 ka (Mendez et al., 2013). As this matches or exceeds the

age of the oldest known H. sapiens fossils, it has been

suggested that the early date could also reflect introgression

from a now extinct species (Mendez et al., 2013).

Hybridization in Eurasia

In the years since the first publication of a relatively high

quality Neanderthal nuclear genome in 2010, it has become

accepted that most extant H. sapiens populations from outside

sub-Saharan African have �2% Neanderthal-derived DNA

(Green et al., 2010). The amount of introgression varies

between populations, with a greater extent observed in Chinese

and Japanese populations (Wall et al., 2013), but this disparity

now appears to be smaller than previously indicated and could

be due to the differential effect of drift acting on separate

populations across Eurasia (Prufer et al., 2014) or to multiple

hybridization events (Vernot & Akey, 2014). Traces of

Neanderthal-derived DNA have even been observed in East

African Maasai and elsewhere in sub-Saharan Africa, but since

there is no evidence that Neanderthals ever lived in Africa, it is

DOI: 10.3109/03014460.2014.922616 Diagnosing Homo sapiens in the fossil record 317

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

most parsimonious to suppose that this introgression derives

from back-migrations from Eurasia (Meyer et al., 2012;

Pickrell et al., 2014; Wall et al., 2013).

In 2010 it was also shown that some populations in south

east Asia and Oceania have an additional component of

introgression, from the Denisovans. This group has so far only

been identified from its DNA, which showed it to be

neither Neanderthal nor H. sapiens (Krause et al., 2010).

The Denisovans seemed at first to be a sister group to

H. sapiens/Neanderthals based on mtDNA (Krause et al.,

2010), but when nuclear DNA was sequenced they were

shown to be more closely related to Neanderthals (Reich

et al., 2010). Although Denisovan remains are so far only

known from Siberia, levels of diversity between the known

mitochondrial genomes suggest that their population size may

have been historically greater than that of the Neanderthals

and, by inference, they were probably once widespread

through south east Asia (Cooper & Stringer, 2013). This fits

with the finding that Denisovan-like DNA is largely found

in extant H. sapiens across the Wallace Line, with the highest

percentage in New Guinean and Australian aborigines, at

�4% (Cooper & Stringer, 2013). Furthermore, recent research

shows that the source of this introgressed DNA was a distinct

sub-population of Denisovans from the one known from

Siberia (Prufer et al., 2014).

Prufer et al. (2014) have now shown that interbreeding also

occurred between Neanderthals and Denisovans and possibly

between the Denisovan lineage and an unknown archaic

hominin. The more we find out, the more it seems that inter-

breeding between taxa was common, albeit at relatively low

levels. The amount of Neanderthal (and Denisovan) DNA in

extant H. sapiens populations is small, which could reflect

relatively few matings, but recent evidence instead suggests

that there was only limited reproductive compatibility

between the two species, despite their evolutionary closeness

(Sankararaman et al. 2014), a scenario which is also

compatible with the lack of mtDNA introgression (Currat &

Excoffier, 2011). This incompatibility seems to have been

particularly related to reduced male fertility and our genes

still show the signs of selection to remove Neanderthal

genetic components responsible for this reduction

(Sankararaman et al., 2014). Of course other barriers to

cross-species breeding, such as low population densities,

geographic and cultural boundaries may also have contributed

to the low component of Neanderthal DNA seen in H. sapiens

today (Currat & Excoffier, 2011). The relatively low levels of

Denisovan DNA on the X chromosome of those H. sapiens

populations where it is present may tell a similar story of

limited inter-fertility (Meyer et al., 2012). Despite the on-

going complications involved in a morphological diagnosis,

it is evident that genetic characterization of our species vs

others is increasingly feasible.

The effect of inter-breeding on phenotype

What effect would inter-breeding with an extinct species have

on phenotype? Based on the evidence so far, the amount of

introgressed DNA originating from Neanderthals and

Denisovans is small and may not be expressed in any of the

gross morphological features of H. sapiens. Some functional

genes are known to be included in Neanderthal-derived DNA,

but so far nothing has been reported that relates to significant

changes in skeletal anatomy. Regions of the H. sapiens

genome that show high levels of selection to retain

Neanderthal genetic input are engaged in such activities as

the building of keratin and sugar metabolism (Sankararaman

et al., 2014). It has been suggested that Neanderthal DNA in

these regions could have been advantageous in helping

H. sapiens to adapt to non-African environments

(Sankararaman et al., 2014; Vernot & Akey, 2014), but

it has also been shown that several alleles associated with

disease risk in H. sapiens seem to be correlated with

the presence of Neanderthal DNA (The Type 2 Diabetes

Consortium, 2013; Sankararaman et al., 2014; Vernot &

Akey, 2014).

It seems unlikely that much of the claimed skeletal

evidence of hybridization that has regularly been cited (e.g.

Trinkaus, 2005, 2011) is really a reflection of introgressed

DNA, not least because several examples date from long after

the time of hypothesized inter-breeding, when levels of

introgressed DNA had probably already fallen away. This

assertion is supported by Fu et al.’s (2013) finding that

Tianyuan (dated to �40 ka) apparently has no more

Neanderthal DNA than extant Chinese people, despite its

supposedly archaic features. In any case, the evidence from

other primate species is that the effects of hybridization are

complex, difficult to interpret and may even be cryptic,

particularly if the specimen in question is not a first

generation hybrid (Ackermann, 2010; Kelaita & Cortes-

Ortiz, 2013).

Conclusion

Based on current research, there are evidently genetic traces

of inter-breeding with at least three extinct human groups. We

can truly be said to be a genetic ‘‘patchwork’’ (Stringer,

2012a), but what does this say about the definition of

H. sapiens? Does some degree of inter-fertility necessarily

falsify a specific difference? Of course the answer to this

question depends on the species definition and, using a strict

biological species concept, the answer would be yes.

However, the utility of this concept for fossil species is

questionable, since in most cases it is impossible to test and

its strict use would negate many currently accepted extant

species divisions as well. Within the primate order there are

many hybridizations in the wild and in zoos between long-

accepted species (Ackermann, 2010; Jolly, 2001; Kelaita &

Cortes-Ortiz, 2013, also reviewed by Winder & Winder, this

volume); indeed Jolly (2001) estimates that inter-fertility

could exist between species up to 4 Ma after their divergence.

Clear and impermeable species divisions may be a useful way

of thinking about the fossil record, but this does not

correspond to biological reality. As Jolly (2001: 129) stated

in comparing the taxonomy of recent papionins and of fossil

hominins,

The message . . . is to concentrate on biology, avoid

semantic traps and realize that any species-level taxonomy

based on fossil material is going to be only an approximate

reflection of real-world complexities.

318 C. B. Stringer & L. T. Buck Ann Hum Biol, 2014; 41(4): 312–322

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Morphometric comparisons of differences in cranial shape

show Neanderthals and H. sapiens (both recent and Upper

Palaeolithic) to be more different than Pan troglodytes and

Pan paniscus (Harvati, 2003) and comparable to differences

found between many other primate species (Harvati et al.,

2004; Lordkipanidze et al., 2013; Stringer, 2012a,b).

Uniting H. sapiens and H. neanderthalensis would also

lack any morphological coherence, since a species

combining Neanderthals and H. sapiens would be diagnosed

simultaneously by a long, low neurocranium and a

high globular neurocranium; by large, continuous supraorbital

tori; and by no continuous supraorbital tori, etc. (Stringer,

2014). This certainly appears unworkable as a species

diagnosis.

Nevertheless, fossil and genetic evidence compiled over

the last few decades show H. sapiens to be a morphologically

variable species and it may, thus, seem that there are not

sufficient features in common to form a cohesive whole.

However, it is important to distinguish between shared species

level traits, which can be seen (in various combinations) in the

fossil record going back hundreds of thousands of years

(derived from a recent African origin) and regional or

‘‘racial’’ traits (added subsequently). The latter category is

largely due to the combined effects of natural selection, drift,

founder effect and sexual selection operating over only the

last 60 ka. H. sapiens share specific traits including a high,

round neurocranium, small face, true chin, small supraorbital

tori and gracile skeleton, but recent H. sapiens from different

regions may also vary further in body shape, skin and hair

colour and the form of the hair, nose, eyes and lips. These

regional traits could potentially be affected by some degree

of archaic introgression, but the evidence so far is that the

phenotypic effects of this are small.

While it certainly seems problematic to cleanly delineate

morphologically recent H. sapiens, anatomical characteriza-

tion of the Homo sapiens lineage should still be possible from

features such as cranial globularity, basicranial flexion, dental

microstructure, inner ear morphology and pelvic shape. The

shape of the parietal region in H. sapiens seems particularly

distinctive (Bruner, 2010; Stringer, 1974, 1978, 2002) and

makes a significant contribution to cranial globularity in both

lateral and occipital views. Basicranial flexion is a complex

feature, but H. sapiens certainly appears distinctive in various

measurements of this (Bastir et al., 2010; Lieberman et al.,

2002). Dental microstructure, especially with the advent of

micro-CT and synchrotron technology, is also revealing clear

differences between early and recent H. sapiens and other

hominin species, in features such as enamel thickness and the

shape of the enamel dentine junction (Crevecoeur et al., 2014;

Smith et al., 2012). Inner ear morphology has long been

recognized as distinguishing between H. sapiens and

H. neanderthalensis, but recent research is increasing reso-

lution, which should also allow discrimination between

H. sapiens and species such as H. heidelbergensis and

H. erectus (Spoor, 2013). Pelvic morphology clearly differ-

entiates an anatomically recent H. sapiens pattern that was

present by at least 100 ka at Skhul and Qafzeh (Rak, 1990),

but the problem here is that the lack of African post-cranial

fossils from the Middle Pleistocene prevents any determin-

ation of when this pattern first appeared.

The discovery of a large sample of Middle Pleistocene

humans in the Sima de los Huesos, Atapuerca (Arsuaga

et al., 1990, 1993; Martinon-Torres et al., 2012) and of

several penecontemporaneous, but distinctive crania from

Dmanisi in Georgia (Gabunia & Vekua, 1995;

Lordkipanidze et al., 2013; Vekua et al., 2002) shows

how little of intra-population variation is typically sampled

in the fossil record. In the case of the Sima sample this has

led to much discussion about its classification (e.g. Gracia-

Tellez et al., 2013; Stringer, 2012c) and, in the case of

Dmanisi, there had been debate over whether the specimens

could all belong to the same species. It has recently been

argued that their level of variation does not exceed that

found in recent H. sapiens or chimpanzees and that it,

therefore, is justifiable to place them in a single species

(Lordkipanidze et al., 2013). Based on the level of variation

described at Dmanisi, the authors went even further in

suggesting that there was insufficient variation in the

African record of early Homo to designate multiple species.

They therefore suggested the sinking of species such as

H. rudolfensis and H. habilis into a polytypic H. erectus

(Lordkipanidze et al., 2013). This conclusion has been

criticized on the grounds that the authors made no attempt

to distinguish between primitive and derived characters, did

not consider the post-cranial evidence (Spoor, 2013) or the

dental evidence and included elderly (edentulous) and

juvenile crania (Hublin, 2014). In addition there was use

of an overly general landmark set for geometric morpho-

metric analyses, which fails to fully distinguish between

some extant non-human primate species (Hublin, 2014). It

has also been asserted that Dmanisi has derived H. erectus

traits not seen in H. habilis or H. rudolfensis and, thus, is

most parsimoniously an early example of H. erectus as

more strictly defined (Spoor, 2013). Finally, even the recent

affirmation that the Dmanisi sample does represent one

variable population has already been challenged on the

basis of its great range in mandibular morphology

(Bermudez de Castro et al., 2014).

We look forward to further increases in the size of fossil

samples for vanished hominin populations in order to assay

their variation more realistically and to improved technology

to scrutinize their morphology in ever-greater detail. The

most significant advances in diagnosing our species, however,

are likely to come from the burgeoning studies of both extant

and extinct genomes. With further research on the function-

ality of DNA differences and of epigenetic controls on the

expression of that DNA (Gokhman et al., 2014), we will

eventually be in a much stronger position to combine our

studies of the genome and phenome in both ancient and living

humans and ultimately determine much more firmly the

boundaries of H. sapiens as a morphologically and genetically

distinct species.

Acknowledgements

CS would like to thank Sarah Elton and Kevin Kuykendall for invitinghim to participate in the SSHB conference in Durham. Both authorswould like to thank Ros Fleming, Jon Buck and two anonymousreviewers for their helpful comments and the Human Origins ResearchFund of the Natural History Museum, London and The CallevaFoundation for funding.

DOI: 10.3109/03014460.2014.922616 Diagnosing Homo sapiens in the fossil record 319

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Declaration of interest

The authors report no conflicts of interest. The authors alone areresponsible for the content and writing of this article.

References

Ackermann RR. 2010. Phenotypic traits of primate hybrids: recognizingadmixture in the fossil record. Evolut Anthropol Issues News Rev 19:258–270.

Arsuaga J-L, Martinez I, Gracia A, Carretero J-M, Carbonell E. 1993.Three new human skulls from the Sima de los Huesos MiddlePleistocene site in Sierra de Atapuerca, Spain. Nature 362:534–537.

Arsuaga JL, Carretero JM, Gracia A, Martınez I. 1990. New discoveriesof human fossils in the Middle Pleistocene site of Atapuerca/Ibeas.Bull Memoir Soc Anthropol Paris 2:93–96.

Aubert M, Pike AWG, Stringer C, Bartsiokas A, Kinsley L, Eggins S,Day M, Grun R. 2012. Confirmation of a late Middle Pleistocene agefor the Omo Kibish 1 cranium by direct uranium-series dating. J HumEvol 63:704–710.

Bailey SE, Weaver TD, Hublin J-J. 2009. Who made the Aurignacianand other early Upper Paleolithic industries? J Hum Evol 57:11–26.

Bar-Yosef Mayer DE, Vandermeersch B, Bar-Yosef O. 2009. Shells andochre in Middle Paleolithic Qafzeh Cave, Israel: indications formodern behavior. J Hum Evol 56:307–314.

Bar-Yosef O, Bordes J-G. 2010. Who were the makers of theChatelperronian culture? J Hum Evol 59:586–593.

Bastir M, Rosas A, Stringer C, Cuetara JM, Kruszynski R, Weber G,Ross C, Ravosa M. 2010. Effects of brain and facial size on basicranialform in human and primate evolution. J Hum Evol 58:424–431.

Bermudez De Castro JM, Martinon-Torres M, Sier MJ, Martın-FrancesL. 2014. On the Variability of the Dmanisi Mandibles. PLoS One 9:e88212.

Blome MW, Cohen AS, Tryon CA, Brooks AS, Russell J. 2012. Theenvironmental context for the origins of modern human diversity: asynthesis of regional variability in African climate 150,000–30,000years ago. J Hum Evol 62:563–592.

Brauer G. 1992. Africa’s place in the evolution of Homo sapiens. In:Brauer G, Smith FH, editors. Continuity or replacement: controversiesin Homo sapiens evolution. Rotterdam: A. A. Balkema. p 83–98.

Brauer G. 2011. Middle Pleistocene diveristy in Africa and the origin ofmodern humans. In: Hublin J-J, McPherron SP, editors. Modernorigins: a North African perspective. Dordrecht: Springer.

Brose DS, Wolpoff MH. 1971. Early Upper Paleolithic man and LateMiddle Paleolithic tools. Am Anthropol 73:1156–1194.

Brumm A, Moore MW. 2005. Symbolic revolutions and the Australianarchaeological record. Cambridge Archaeol J 15:157–175.

Bruner E. 2010. The evolution of the parietal cortical areas in the humangenus: between structure and cognition. In: Broadfield D, Yuan M,Schick K, Toth N, editors. The human brain evolving:Palaeoneurological studies in honour of Ralph L. Holloway.Gosport, IN: Stone Age Institute Press.

Buck LT, Stock JT, Foley RA. 2010. Levels of intraspecific variationwithin the catarrhine skeleton. Int J Primatol 31:779–795.

Cooper A, Stringer CB. 2013. Did the Denisovans Cross Wallace’s Line?Science 342:321–323.

Coulthard TJ, Ramirez JA, Barton N, Rogerson M, Brucher T. 2013.Correction: were rivers flowing across the Sahara during the lastinterglacial? Implications for human migration through Africa. PLoSOne 8:e74834.

Crevecoeur I, Semal P, Brooks AS. 2010. The Late Stone Age humanremains from Ishango (Democratic Republic of Congo). Contributionto the study of the African Late Pleistocene modern human diversity.Am J Phys Anthropol S50:87.

Crevecoeur I, Skinner MM, Bailey SE, Gunz P, Bortoluzzi S, Brooks AS,Burlet C, et al. 2014. First early hominin from Central Africa(Ishango, Democratic Republic of Congo). PLoS One 9:e84652.

Currat M, Excoffier L. 2011. Strong reproductive isolation betweenhumans and Neanderthals inferred from observed patterns of intro-gression. Proc Natl Acad Sci USA 108:15129–15132.

D’errico F, Stringer C. 2011. Evolution, revolution or saltation scenariofor the emergence of modern cultures? Philos Trans R Soc B Biol Sci366:1060–1069.

Day M, Stringer CB. 1982. A reconsideration of the Omo Kibish remainsand the erectus-sapiens transition. Nice: Pretirage First InternationalCongress of Human Palaeontology. p 814–846.

Day MH, Stringer CB. 1991. Les restes craniens d’Omo Kibish et leurclassification a l’interieur du genre Homo. L’Anthropol 94:573–594.

Finlayson C. 2013. Viewpoint: human evolution, from tree to braid.Available online at: http://www.bbc.co.uk/news/science-environment-25559172#, accessed January 15, 2014.

Finlayson C, Brown K, Blasco R, Rosell J, Negro JJ, Bortolotti GR,Finlayson G, et al. 2012. Birds of a feather: Neanderthal exploitationof raptors and corvids. PLoS One 7:e45927.

Foley R, Lahr MM. 1997. Mode 3 technologies and the evolution ofmodern humans. Cambridge Archaeol J 7:3–36.

Fu Q, Meyer M, Gao X, Stenzel U, Burbano HA, Kelso J, Paabo S. 2013.DNA analysis of an early modern human from Tianyuan Cave, China.Proc Natl Acad Sci USA 110:2223–2227.

Gabunia L, Vekua A. 1995. A Plio-Pleistocene hominid from Dmanisi,East Georgia, Caucasus. Nature 373:509–512.

Gokhman D, Riancho JA, Kelso J, Paabo S, Meshover E, Carmel L.2014. Reconstructing the DNA methylation maps of the Neanderthaland the Denisovan. Science 344:523–527.

Gracia-Tellez A, Arsuaga J-L, Martınez I, Martın-Frances L, Martinon-Torres M, Bermudez De Castro J-M, et al. 2013. Orofacial pathologyin Homo heidelbergensis: the case of Skull 5 from the Sima de losHuesos site (Atapuerca, Spain). Quaternary Int 295:83–93.

Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M,Patterson N, et al. 2010. A Draft Sequence of the Neandertal Genome.Science 328:710–722.

Grun R, Stringer C, McDermott F, Nathan R, Porat N, Robertson S,Taylor L, et al. 2005. U-series and ESR analyses of bones and teethrelating to the human burials from Skhul. J Hum Evol 49:316–334.

Hammer M, Woerner A, Mendez F, Watkins J, Wall J. 2011. Geneticevidence for archaic admixture in Africa. Proc Natl Acad Sci USA108:15123–15128.

Harvati K. 2003. The Neanderthal taxonomic position: models of intra-and inter-specific craniofacial variation. J Hum Evol 44:107–132.

Harvati K, Frost SR, Mcnulty KP. 2004. Neanderthal taxonomyreconsidered: Implications of 3D primate models of intra- andinterspecific differences. Proc Natl Acad Sci USA 101:1147–1152.

Harvati K, Stringer C, Grun R, Aubert M, Allsworth-Jones P, FolorunsoCA. 2011. The Later Stone Age calvaria from Iwo Eleru, Nigeria:morphology and chronology. PLoS One 6:e24024.

Harvati K, Stringer C, Grun R, Aubert M, Allsworth-Jones P, FolorunsoCA. 2013. Correction: The Later Stone Age Calvaria from Iwo Eleru,Nigeria: morphology and chronology. PLoS One 8: 10.1371/annota-tion/887b6c18-6c37-44d2-8a50-2760bc9ad5d6.

Hawks J. 2010. Neandertals Live! Available online at: http://johnhawks.net/weblog/reviews/neandertals/neandertal_dna/neandertals-live-genome-sequencing-2010.html, accessed 2010.

Higham T, Jacobi R, Julien M, David F, Basell L, Wood R, Davies W,Ramsey CB. 2010. Chronology of the Grotte du Renne (France) andimplications for the context of ornaments and human remains withinthe Chatelperronian. Proc Natl Acad Sci USA 107:20234–20239.

Howells WW. 1973. Cranial variation in man: a study by multivariateanalysis of patterns of difference among recent human populations.Cambridge, MA: Harvard University Press.

Hublin J-J. 2007. What can Neanderthals tell us about modern humanorigins? In: Mellars P, Boyle K, Bar-Yosef O, Stringer C, editors.Rethinking the human revolution. Cambridge: McDonald InstituteMonographs.

Hublin J-J. 2014. Palaeoanthropology: Homo erectus and the limits of aPaleontological species. Curr Biol 24:R82–R84.

Jolly CJ. 2001. A proper study for mankind: analogies from the Papioninmonkeys and their implications for human evolution. Am J PhysAnthropol 116:177–204.

Kelaita MA, Cortes-Ortiz L. 2013. Morphological variation of genetic-ally confirmed Alouatta pigra x A. palliata hybrids from a naturalhybrid zone in Tabasco, Mexico. Am J Phys Anthropol 150:223–234.

King WBR. 1864. The reputed fossil man of the Neanderthal. Q J Sci1:88–97.

Klein RG. 2000. Archaeology and the evolution of human behaviour.Evol Anthropol 9:17–36.

Klein RG. 2008. Out of Africa and the evolution of human behaviour.Evol Anthropol 17:267–281.

320 C. B. Stringer & L. T. Buck Ann Hum Biol, 2014; 41(4): 312–322

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Krause J, Fu Q, Good JM, Viola B, Shunkov MV, Derevianko AP, PaaboS. 2010. The complete mitochondrial DNA genome of an unknownhominin from southern Siberia. Nature 464:894–897.

Lachance J, Vernot B, Elbers CC, Ferwerda B, Froment A, Bodo J-M,Lema G, et al. 2012. Evolutionary history and adaptation from high-covereage whole-genome sequences of diverse African hunter-gath-erers. Cell 457:457–469.

Lahr MM. 1996. The evolution of modern human diversity: a study ofcranial variation. Cambridge: Cambridge University Press.

Lieberman DE, McBratney BM, Krovitz G. 2002. The evolution anddevelopment of cranial form in Homo sapiens. Proc Natl Acad SciUSA 99:1134–1139.

Lordkipanidze D, Ponce De Leon MS, Margvelashvili A, Rak Y,Rightmire PG, Vekua A, Zollikofer CPE. 2013. A complete skull fromDmanisi, Georgia, and the evolutionary biology of early Homo.Science 342:326–331.

Martinon-Torres M, Bermudez De Castro JM, Gomez-Robles A, Prado-Simon L, Arsuaga J-L. 2012. Morphological description and com-parison of the dental remains from Atapuerca-Sima de los Huesos site(Spain). J Hum Evol 62:7–58.

McBrearty S, Brooks AS. 2000. The revolution that wasn’t: a newinterpretation of the origin of modern human behavior. J Hum Evol39:453–563.

McBrearty SS, Stringer C. 2007. The coast in colour. Nature 449:793–794.

Mellars P, Stringer C. 1989. The human revolution: behavioural andbiological perspectives in the origins of modern humans. Edinburgh:Edinburgh University Press.

Mendez FL, Krahn T, Schrack B, Krahn A-M, Veeramah KR, WoernerAE, Fomine FLM, et al. 2013. An African American paternal lineageadds an extremely ancient root to the human Y chromosomephylogenetic tree. Am J Hum Genet 92:454–459.

Meyer M, Kircher M, Gansauge M-T, Li H, Racimo F, Mallick S,Schraiber JG, et al. 2012. A high-coverage genome sequence from anarchaic Denisovan individual. Science 338:222–226.

Notton D, Stringer C. 2010. Who is the type of Homo sapiens? [Online].Available online at: http://iczn.org/content/who-type-homo-sapiens,accessed January 15, 2014.

O’Connell JF, Allen J. 2007. Pre-LGM Sahul (Pleistocene Australia-NewGuinea) and the archaeology of early modern humans. In: Mellars P,Boyle K, Bar-Yosef O, Stringer C, editors. Rethinking the humanrevolution. Cambridge: McDonald Institute for ArchaeologicalResearch. p 395–410.

Peresani M, Fiore I, Gala M, Romandini M, Tagliazcozzo A. 2011. LateNeanderthals and the intentional removal of feathers as evidencedfrom bird bone taphonomy at Fumane Cave 44 ky B.P, Italy. Proc NatlAcad Sci USA 108:3888–3893.

Pickrell JK, Patterson N, Loh P-R, Lipson M, Berger B, Stoneking M,Pakendorf B, Reich D. 2014. Ancient west Eurasian ancestry insouthern and eastern Africa. Proc Natl Acad Sci USA 111:2632–2637.

Prufer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S,Heinze A, et al. 2014. The complete genome sequence of aNeanderthal from the Altai Mountains. Nature 505:43–49.

Rak Y. 1990. On the differences between two pelvises of Mousteriancontext from the Qafzeh and Kebara caves, Israel. Am J PhysAnthropol 81:323–332.

Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, ViolaB, et al. 2010. Genetic history of an archaic hominin group fromDenisova Cave in Siberia. Nature 468:1053–1060.

Rendu W, Beauval C, Crevecoeur I, Bayle P, Balzeau A, Bismuth T,Bourguignon L, et al. 2013. Evidence supporting an intentionalNeandertal burial at La Chapelle-aux-Saints. Proc Natl Acad Sci USA111:81–86.

Salomon H, Vignaud C, Coquinot Y, Beck L, Stringer C, Strivay D,D’errico F. 2012. Selection and heating of colouring materials in theMousterian level of Es-Skhul (c. 100,000 years BP, Mount Carmel,Israel). Archaeometry 54:698–722.

Sankararaman S, Mallick S, Dannemann M, Prufer K, Kelso J, Paabo S,Patterson N, Reich D. 2014. The genomic landscape of Neanderthalancestry in present-day humans. Nature 508:354–357.

Schwartz JH, Tattersall I. 2000. The human chin revisited: what is it andwho has it? J Hum Evol 38:367–409.

Shea JJ, Fleagle JG, Assefa Z. 2007. Context and chronology of earlyHomo sapiens fossils from the Omo Kibish Formation, Ethiopia. In:Mellars P, Boyle K, Bar-Yosef O, Stringer S, editors. Rethinking the

human revolution. Cambridge: McDonald Institute for ArchaeologicalResearch.

Smith F. 1992. The role of continuity in modern human origins. In:Brauer G, Smith F, editors. Continuity or replacement? Controversiesin Homo sapiens evolution. Rotterdam: Balkema. p 145–156.

Smith TM, Olejniczak AJ, Zermeno JP, Tafforeau P, Skinner MM,Hoffmann A, Radovcic J, et al. 2012. Variation in enamel thicknesswithin the genus Homo. J Hum Evol 62:395–411.

Spoor F. 2013. Small-brained and big-mouthed. Nature 502:452–453.Stearn WT. 1959. The background of linnaeus’s contributions to the

nomenclature and methods of systematic biology. Syst Zool 8:4–22.Stewart JR, Stringer CB. 2012. Human evolution out of Africa: the role

of refugia and climate change. Science 335:1317–1321.Stringer C. 1974. Population relationships of later Pleistocene hominids:

a multivariate study of available crania. J Archaeol Sci 1:317–342.Stringer C. 2002. Modern human origins: progress and prospects. Phil

Trans R Soc B Biol Sci 357:563–579.Stringer C. 2003. Human evolution: out of Ethiopia. Nature 423:

692–693, 695.Stringer C. 2012a. What makes a modern human. Nature 485:33–35.Stringer C. 2012b. The origin of our species. London: Penguin.Stringer C. 2012c. The status of Homo heidelbergensis (Schoetensack

1908). Evol Anthropol 21:101–107.Stringer C. 2014. Why we are not all multiregionalists now. Trends Ecol

Evol 29:248–251.Stringer CB. 1978. Some problems in Middle and Upper Pleistocene

hominid relationships. In: Chivers D, Joysey K, editors. Recentadvances in Primatology. London: Academic Press.

Stringer CB. 1994. Out of Africa – a personal history. In: Nitecki M,Nitecki DV, editors. Origins of anatomically modern humans. NewYork: Plenum Press.

Stringer CB. 1996. Current issues in modern human origins. In: MeikleWE, Howell FC, Jablonski NG, editors. Contemporary issues inhuman evolution. San Francisco, CA: California Academy ofSciences.

Stringer CB, Finlayson JC, Barton RNE, Fernandez-Jalvo Y, Cacares I,Sabin RC, Rhodes EJ, et al. 2008. Neanderthal exploitation of marinemammals in Gibraltar. Proc Natl Acad Sci USA 105:14319–14324.

Stringer CB, Hublin J-J, Vandermeersch B. 1984. The origin ofanatomically modern humans in Western Europe. In: Smith F,Spencer F, editors. The origins of modern humans. New York: Liss.

The Type 2 Diabetes Consortium. 2013. Sequence variants in SLC16A11are a common risk factor for type 2 diabetes in Mexico. Nature506:97–101.

Trinkaus E. 2005. Early modern humans. Annu Rev Anthropol 34:207–230.

Trinkaus E. 2011. Late Neandertals and early modern humans in Europe,population dynamics and Paleobiology. In: Condemi S, Weniger G-C,editors. Continuity and discontinuity in the peopling of Europe: onehundred and fifty years of Neanderthal study. Dordretch: Springer.

Vanhaeren M, D’errico F, Stringer C, James S, Todd J, Mienis H. 2006.Middle Paleolithic Shell Beads in Israel and Algeria. Science 312:1785–1788.

Vekua A, Lordkipanidze D, Rightmire GP, Agusti J, Ferring R,Maisuradze G, Mouskhelishvili A, et al. 2002. A new skull of earlyHomo from Dmanisi, Georgia. Science 297:85–89.

Vernot B, Akey JM. 2014. Resurrecting surviving neandertal lineagesfrom modern human genomes. Science 343:1017–1021.

Von Cramon-Taubadel N. 2009. Revisiting the homoiology hypothesis:the impact of phenotypic plasticity on the reconstruction ofhuman population history from craniometric data. J Hum Evol 57:179–190.

Wall JD, Yang MA, Jay F, Kim SK, Durand EY, Stevison LS, GignouxC, et al. 2013. Higher levels of Neanderthal ancestry in East Asiansthan Europeans. Genetics 194:199–209.

White TD, Asfaw B, Degusta D, Gilbert H, Richards GD, Suwa G, ClarkHowell F. 2003. Pleistocene Homo sapiens from Middle Awash,Ethiopia. Nature 426:742–747.

Winder IC, Winder NP. this volume. Reticulate evolution and the humanpast: an anthropological perspective. Ann Hum Biol 41.

Wolpoff MH. 1986. Describing anatomically modern Homo sapiens: adistinction without a definable difference. Anthropos 23:41–53.

Wolpoff M, Caspari R. 1997a. What does it mean to be modern? In:Clark GA, Willermet CM, editors. Conceptual issues in modernhuman origins research. New York: Aldine de Gruyter.

DOI: 10.3109/03014460.2014.922616 Diagnosing Homo sapiens in the fossil record 321

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.

Wolpoff MH, Caspari R. 1997b. Race and human evolution. New York:Simon and Schuster.

Wolpoff MH, Thorne AG, Smith FH, Frayer DW, Pope GG. 1994.Multiregional evolution: a world- wide source for modern humanpopulations. In: Nitecki MH, Nitecki DV, editors. Origins ofanatomically modern humans. New York: Plenum.

Ziegler M, Simon MH, Hall IR, Barker S, Stringer C, Zahn R. 2013.Development of Middle Stone Age innovation linked to rapid climatechange. Nat Commun 4:1905.

Zilhao J, Angelucci DE, Badal-Garcıa E, D’errico F, Daniel F, Dayet L,Douka K, et al. 2010. Symbolic use of marine shells and mineralpigments by Iberian Neandertals. Proc Natl Acad Sci USA 107:1023–1028.

Zilhao J, D’errico F, Bordes J-G, Lenoble A, Texier J-P, Rigaud J-P.2006. Analysis of Aurignacian interstratification at theChatelperronian-type site and implications for the behavioralmodernity of Neandertals. Proc Natl Acad Sci USA 103:12643–12648.

322 C. B. Stringer & L. T. Buck Ann Hum Biol, 2014; 41(4): 312–322

Ann

Hum

Bio

l Dow

nloa

ded

from

info

rmah

ealth

care

.com

by

Nat

ural

His

tory

Mus

eum

on

06/3

0/14

For

pers

onal

use

onl

y.