The Hybrid Origin of “Modern” Humans

Abstract

Recent genomic research has shown that hybridization between substantially diverged lineages is the rule, not the exception, in human evolution. However, the importance of hybridization in shaping the genotype and phenotype of Homo sapiens remains debated. Here we argue that current evidence for hybridization in human evolution suggests not only that it was important, but that it was an essential creative force in the emergence of our variable, adaptable species. We then extend this argument to a reappraisal of the archaeological record, proposing that the exchange of cultural information between divergent groups may have facilitated the emergence of cultural innovation. We discuss the implications of this Divergence and Hybridization Model for considering the taxonomy of our lineage.

Full text

SYNTHESIS PAPER
The Hybrid Origin of ‘‘Modern’’ Humans
Rebecca Rogers Ackermann
1
•Alex Mackay
1,2
•Michael L. Arnold
3
Received: 12 August 2015 / Accepted: 14 September 2015
ÓSpringer Science+Business Media New York 2015
Abstract Recent genomic research has shown that
hybridization between substantially diverged lineages is
the rule, not the exception, in human evolution. However,
the importance of hybridization in shaping the genotype
and phenotype of Homo sapiens remains debated. Here we
argue that current evidence for hybridization in human
evolution suggests not only that it was important, but that it
was an essential creative force in the emergence of our
variable, adaptable species. We then extend this argument
to a reappraisal of the archaeological record, proposing that
the exchange of cultural information between divergent
groups may have facilitated the emergence of cultural
innovation. We discuss the implications of this Divergence
and Hybridization Model for considering the taxonomy of
our lineage.
Keywords Cultural and biological modernity 
Hybridization Frontiers Neanderthals Denisovans
Hybridization Acts as a Powerful Force Driving
Diversification and Evolutionary Innovation
Hybridization is ubiquitous, occurring in almost all sexu-
ally reproducing groups of organisms (Dowling and Secor
1997; Mallet 2005; Arnold and Meyer 2006), and resulting
in the transfer of genes from one population to another
(gene flow). Historically, researchers tended to think of
gene flow (via migration, etc.) and drift as evolutionary
forces that have genome-wide effects (Slatkin 1985).
Broadly, this means that gene flow should cause popula-
tions to become more similar (decrease inter-taxon varia-
tion), and genetic drift more distinct (increase inter-taxon
variation), making it difficult for one to imagine a role for
gene flow in scenarios of diversification (Slatkin 1985). But
in reality, divergence across the genome accompanied by
gene flow has been shown to be widespread albeit
heterogeneous (Nosil and Feder 2012). Moreover, gene
flow can affect separate regions of the genome quite dif-
ferently, depending on the degree of differentiation of the
hybridizing lineages at loci of interest (Key 1968; Harrison
1986;Wu2001). Hybridization, and the resultant gene
flow, therefore works in conjunction with other evolu-
tionary processes that act to diversify populations, though it
can be difficult to predict its effects without knowledge
about genetic diversification in the hybridizing lineages
(Seehausen et al. 2014).
The consequences of hybridization vary widely, and
include: the merger of evolutionarily distinct lineages, the
evolution of reproductive isolation between lineages, the
evolution of novel phenotypes, the formation of stable hy-
brid zones, the extinction of one or both hybridizing lin-
eages, and the evolution of new species (Arnold 1992;
Seehausen 2004). Arguably the hallmark of hybridization
is an increase in biological variation, due to novel
&Rebecca Rogers Ackermann
becky.ackermann@uct.ac.za
1
Department of Archaeology, University of Cape Town,
Rondebosch, South Africa
2
Centre for Archaeological Science, University of
Wollongong, Wollongong, Australia
3
Department of Genetics, University of Georgia, Athens, GA,
USA
123
Evol Biol
DOI 10.1007/s11692-015-9348-1

amalgamations of traits. Populations with wide ranges of
both genetic and phenotypic variation have been demon-
strated in a number of organisms. Hybrid populations can
contain individuals that are intermediate to parents, ones
that resemble parents (cryptic hybrids), or individuals that
fall outside of the range of parental forms (transgressive
hybrids) (Seehausen et al. 2014). Transgression can be
particularly striking, and is one way in which hybrids may
succeed in places where their parents do not. In this
manner, hybridization stands as an important producer of
evolutionary innovation, which in certain circumstances
can result in increased fitness and evolutionary success
(Arnold and Meyer 2006; Seehausen et al. 2014).
Molecular Data Provide a Growing Body
of Evidence for Hybrid Origins of Modern People
In the case of humans, just as in other sexually-reproducing
organisms, gene flow has occurred repeatedly in our past.
The evidence we have to date indicates that the divergence
of lineages (e.g. Neanderthal, Denisovan, African) known
to play a role in modern human ancestry is relatively
recent, occurring over the course of the past one million
years or slightly more (Krause et al. 2010; Prufer et al.
2014). Researchers have detected signatures of past
hybridization events among these lineages (Green et al.
2010; Fu et al. 2014,2015; Prufer et al. 2014; Seguin-
Orlando et al. 2014). For example, there is evidence for
admixture—possibly in the Middle East—between Nean-
derthals and people expanding from Africa circa 47–65 ka
(Sankararaman et al. 2012). In Siberia, this admixture
window has been estimated at 50–60 ky (Fu et al. 2014),
while in Romania admixture occurred as recently as
*40,000 years ago (Fu et al. 2015). As a result, Nean-
derthal genomic material has been identified in all extant
non-African populations of H. sapiens (Fu et al. 2013),
with these populations containing *1–4 % Neanderthal
genes (Green et al. 2010), and *20 % of the Neanderthal
genome represented in total (Vernot and Akey 2014). In
contrast, Denisovan introgression apparently impacted
primarily Oceanic and Asian H. sapiens populations
(Meyer et al. 2012); as much as 7 % of chromosome 21
from present-day Papuan individuals derives from
Denisovans (Fu et al. 2013). Adding to the picture of
reticulate evolution within recent Homo, Prufer et al.
(2014) inferred introgression between Neanderthals and
Denisovans as well as from an unidentified hominin into
the Denisovan lineage, and suggested that gene flow events
in both directions were likely less discrete and therefore
more complex (Prufer et al. 2014). Denisovan-like mito-
chondrial DNA has also been detected in earlier (ca.
400,000-year old) ‘Sima de los Huesos’ hominins living in
northern Spain (Meyer et al. 2014), prior to the origin of
our lineage. Introgressive hybridization among Homo lin-
eages was not restricted to regions outside of Africa
(Veeramah and Hammer 2014). Within Africa, two studies
have provided evidence for introgressive hybridization
between modern sub-Saharan African groups and a now
extinct (and unknown) hominin taxon (Hammer et al. 2011;
Lachance et al. 2012). In the first, introgression was esti-
mated to have occurred ca. 35,000 years before present
between lineages that diverged approximately 0.7 Ma,
resulting in a small amount (2 %) of ancient genetic
material in modern sub-Saharan hunter-gatherer popula-
tions (Hammer et al. 2011). In the second, whole-genome
sequencing of fifteen individuals from three different
hunter-gatherer populations detected ancient introgressive
hybridization from an unknown archaic population or
populations (Lachance et al. 2012).
Researchers are also increasingly taking the stance that
while interbreeding among multiple hominin groups within
and outside of Africa in the Late Pleistocene resulted in
fairly low frequencies of introgressed genes in extant
humans (due to infrequent interbreeding, reduced fitness of
early-generation hybrid individuals or demographic
parameters), genes exchanged through interbreeding had
important effects on fitness outcomes in the past and
human well-being today (Callaway 2015). As with any
introgressive hybridization, much of the genomic material
transferred was undoubtedly neutral (Key 1968). There is
also evidence that some of the Neanderthal contribution to
recent human genomes has been selected against, possibly
due to genetic incompatibilities (Sankararaman et al.
2014). In other circumstances introgression appears to have
produced novel genetic combinations that were adaptively
beneficial to local populations (e.g. Prufer et al. 2014;
Sankararaman et al. 2014; Vernot and Akey 2014). These
emerging studies raise the possibility that hybridization
played not merely a small or ephemeral role, but a central
role in the emergence and evolution of Homo sapiens
through the introduction of new variation, and production
of new genetic amalgamations and innovation, thereby
opening up more evolutionary possibilities.
For example, Neanderthal genes related to keratin pro-
duction, thereby affecting skin and hair phenotypes, have
been retained in humans living today (e.g. Sankararaman
et al. 2014; Vernot and Akey 2014), suggesting that
hybridization and subsequent introgression facilitated the
expansion of African people into previously unexplored,
non-African territories with decidedly different climatic
conditions. Consistent with this inference are signatures of
positive selection for the chromosomal regions carrying
genes affecting the cellular response to ultraviolet irradia-
tion (Ding et al. 2014). Similarly, the presence of
Denisovan and Neanderthal human leucocyte antigen
Evol Biol
123

(HLA) haplotypes in living Oceanian and Eurasian popu-
lations, respectively, suggests the acquisition and retention
of variants from populations whose immune systems were
better adapted to local pathogens (Abi-Rached et al. 2011),
supporting the argument that immune-related loci appear to
benefit significantly from the introduction of new genetic
diversity through hybridization (Key et al. 2014;Se
´gurel
and Quintana-Murci 2014). Genes involved in innate
immunity (i.e. immune surveillance and reactivity) have
also been transferred from archaic groups (Dannemann
et al. 2015). Haplotypes underlying adaptations necessary
for living in the low-oxygen environment of the high-alti-
tude Tibetan plateau also originated from introgression and
demonstrate genetic variation indicative of positive,
directional selection (Huerta-Sa
´nchez et al. 2014).
Retained introgressed alleles are also implicated in a
number of modern-day human diseases (e.g. autoimmune
disorders, biliary cirrhosis, prostate cancer, type 2 diabetes;
Ding et al. 2014; Sankararaman et al. 2014). The fact that
these diseases tend to occur later in life suggests that these
introgressed alleles were effectively neutral, having little
effect on fitness. It is also possible that characteristics
associated with these diseases were beneficial in the past,
but are not beneficial today with our current lifestyle,
environment and longevity. It is tempting to think of the
presence of ca. 2 % of introgressed genes in living people
as a minor contribution, but in absolute terms it is a con-
siderable amount of retained genes, especially given that
tens of thousands of years have passed since these
hybridization events. Moreover, these genes have provided
our species with the ability to migrate to, and succeed in,
numerous new environments, with different genes intro-
gressed in different contexts, indicating that gene flow has
been responsible for key aspects of human variation (dif-
ferent disease phenotypes, skin properties, etc.). We sus-
pect, based on the current trend but also analogues in living
organisms, that genetic signatures of more hybridization
events will be discovered at an accelerating rate, will
indicate that the exchange of genes among taxa was com-
plex and bi(multi)-directional, and will continue to expand
the time period and geographical extent of these events.
With additional data from many more current and ancient
samples of Homo, estimates of the magnitude of adaptive
and non-adaptive introgression and its effects will be made
possible.
Fossil Data also Support Ongoing Process
of Genetic Exchange in Our Lineage
The fossil record of human evolution also supports a sce-
nario of repeated hybridization. In fact, a wide range of
variation and the emergence of phenotypic novelty—key
signatures present throughout this time period—suggest
that the prevalence of gene exchange may be considerably
more than currently reflected in the genetic data (not
unexpected given the low number of archaic individuals
sequenced to date). Indeed, the Middle to Late Pleistocene
is well-known to be a time of considerable morphological
variation in Homo both inside and outside of Africa. The
wide range of variation in traits, as well as diagnosable (if
not necessarily adaptive; Weaver et al. 2007; Pearson
2013) differences among geographic regions, has led to a
tendency by many towards the recognition of numerous
species (e.g. H. sapiens, H. neanderthalensis, H. heidel-
bergenesis, H. antecessor, H. helmei, H. rhodesiensis).
Moreover, individuals with modern morphology begin to
appear in the African fossil record ca. 200 kya (McDougall
et al. 2005; Rightmire 2009), but this occurs in a piecemeal
fashion, with a mixture of modern and archaic traits per-
sisting in the fossil record in Africa and the Middle East
until after 35 kya (Bra
¨uer 2008; Rightmire 2009), and with
many of the taxa listed above containing individuals with
such mixed morphology. Indeed, in Europe in the late
Pleistocene, where the densest record of multiple forms of
ancient humans exists, this is especially evident, with lar-
gely modern skeletal remains sometimes exhibiting iso-
lated Neanderthal-like features, and vice versa (Duarte
et al. 1999; Trinkaus 2007; Ramirez Rozzi et al. 2009;
Ahern et al. 2013; Smith 2013). Additionally, evidence for
mild developmental disruptions and novel traits consistent
with hybridization exist in one region of the world where
Neanderthals and migrating Africans would have met and
interbred (Ackermann 2010; Ackermann et al. 2006,2014).
Although a handful of individuals have been predicted to
be hybrids on the basis of transgressive phenotypes and
mosaic morphology, it is the identification of a human with
a recent Neanderthal ancestor (4–6 generations prior) based
on sequence data (Fu et al. 2015) that has bolstered the
credibility of previous suggestions that certain individual
fossils are hybrids. This specimen, Pes¸tera cu Oase 1, as
well as Pes¸tera cu Oase 2, were predicted to be hybrids on
the basis of both mosaic morphology and atypical trait
variation (Rougier et al. 2007; Ackermann 2010; Trinkaus
2013). This provides further confirmation that transgressive
phenotypes and mosaic morphology are indeed signatures
of hybridization in hominins, and opens the door for further
investigation into the affinities of purported hybrids (e.g.
Brau
¨er 1981; Duarte et al. 1999; Wolpoff et al. 2001;
Soficaru et al. 2006; Rougier et al. 2007; Ackermann 2010;
Condemi et al. 2013; Curnoe et al. 2015) across the middle-
to-latest Pleistocene. Clearly fossil evidence for admixture
is likely to be more widespread than we currently appre-
ciate, a conclusion also supported by evidence for the
prevalence of atypical traits in other hominin individuals
(Wu et al. 2013).
Evol Biol
123

Taken together, the genetic and morphological evidence
suggest that hybridization between divergent lineages has
occurred numerous times both within and outside of Africa,
and that it has resulted in novel combinations of traits
including amalgamations that provide adaptive benefits to
people living today. This indicates that hybridization
played a significant role in the evolution of our lineage.
Although the consequences of hybridization have largely
been espoused in the genetic literature, they undoubtedly
also include key morphological traits, perhaps even
including ones we associate with ‘‘modernity.’’ This
doesn’t imply that all introgressed genomic segments had
fitness enhancing effects. As discussed above, many were
likely neutral, and some deleterious, potentially resulting in
reduced fitness in some hybrids. For example, the reduced
Neanderthal ancestry in genes on the X chromosome and
those expressed in testes provides some support for a pat-
tern of decreased fertility in male hybrids and selection
against introgressed genetic material (Sankararaman et al.
2014). However, even in circumstances where hybrids have
a lower fitness than the parent species, it is possible that the
high sociality of Homo (often recognized as a trait
indicative of the uniqueness of humans among animals)
could have allowed for an environment where hybrids
would have an increased probability of surviving until
reproduction, with subsequent loss of deleterious alleles in
backcrossed progeny.
A Divergence and Hybridization Model
for the Emergence of Our Species Does Not Align
with Simple Notions of ‘‘Modernity’’
In this light, we view the emergence of biologically mod-
ern humans as an ongoing process that included genetic
exchange throughout much of its evolutionary history. The
variable (and not easily characterisible) nature of the fossil
record of the last million years, combined with the
emerging genetic evidence, suggests that this genetic
exchange across Homo taxa occurred both before and after
the origin of what systematists would call H. sapiens (see
also ‘‘Appendix 1’’). Without this gene flow our species
may have evolved, but it would probably not be H. sapiens
as we know it, with its wide phenotypic variation and
capacity for migration and adaptability in new contexts.
Indeed, it is quite plausible that our species could not have
succeeded outside of Africa to the extent that it did without
hybridization.
Our view of the emergence of our species differs in key
respects to more mainstream views depicted in ‘‘Appendix
1’’, and instead more closely aligns with Darwin’s view of
a continuum between varieties and species under the con-
stant if low-level influence of gene exchange (Mallet
2008). Gene flow was not the only evolutionary process
acting on H. sapiens, and was not responsible for the
diversity of this lineage in its entirety, but nonetheless
played an important role in producing the diverse people
we are today. Our Divergence and Hybridization Model is
most similar to Smith’s Assimilation Model (Smith 2010),
and to a lesser extent Brau
¨er’s Afro-European sapiens
hypothesis (Brau
¨er 1985), but differs in that we consider
the admixture to be significant and unlikely to be limited in
its temporal and/or spatial context. Instead, admixture
happened repeatedly among taxa, both inside and outside
of Africa, resulting in a complex lineage that is not easily
parcelled into discrete taxa despite evidence for substruc-
turing. Because of this dynamic, and the still-to-be-under-
stood phenotypic effects of repeated gene exchange, it is
also a lineage where it becomes problematic to point to a
single place and time for the emergence of ‘‘modernity.’’
Hybridization Can Also Explain Variation
and Innovation Associated with the Emergence
of Modern Culture
We would also argue that the repeated contact of divergent
groups is likely, in many instances, to have resulted in
cultural exchange and innovation, and may have played a
role in the emergence of modern culture. Ethnographic
evidence from frontier societies shows that areas of contact
are interaction zones, where different aspects of culture and
society recombine both across the landscape and over time,
resulting in a variety of outcomes including the loss of
culture, as well as cultural repackaging and innovation
(Lightfoot and Martinez 1995). Creolization has been
shown to result in the construction of new cultures and
identities that replace prior forms (Cohen 2007). These
contact zones may also foster the evolution of overt
markers of cultural group membership (McElreath et al.
2003). In the recent archaeological past, disruptions such as
the spread of agro-pastoralism led to the emergence of
innumerable distinct culture-evolutionary pathways, in
some cases including the appearance of hybrid subsistence
patterns (Sadr 2003). In all of these contexts the outcome
of cultural admixture includes evidence for increased
variation, new combinations of features, and the production
of novelty. Although there is considerable debate sur-
rounding the emergence of modern culture, there is little
doubt that its hallmark is innovation and novelty, as rep-
resented by archaeological evidence for the emergence of
complex multi-part tools, sophisticated technical struc-
tures, symbolism and ornamentation, among other things.
Moreover, relative to the technological complexes that
preceded it (e.g. Acheulean), which appear to have been
fairly homogenous/static, the technology of the last few
Evol Biol
123

hundreds of thousands of years is variable both geo-
graphically and temporally (McBrearty and Brooks 2000).
With regard to the advent of clearly modern culture, it is
worth exploring the possibility that some signatures of
what has traditionally been called ‘modernity’ are the result
of interaction. For example, H. sapiens and Neanderthals
occupied a fluctuating border for tens of thousands of years
in the Levant (Tchernov 1994), without either habitually
expressing the combination of technological, ornamental
and artistic traits that are typically accepted as the signature
of modern human behaviour. This is despite evidence
suggesting that the capacity for such culture was already
present (and perhaps even ancestral, Joordens et al. 2015)
in both populations (Vanhaeren et al. 2006; Bouzouggar
et al. 2007; Bar-Yosef Mayer et al. 2009; Peresani et al.
2011; Peresani et al. 2013; Rodrı
´guez-Vidal et al. 2014).
The later expansion of H. sapiens populations deeper into
west Asia and Europe, however, probably induced novel
developments in Neanderthal behaviours (Hublin et al.
2012; Higham et al. 2014) and was characterised by an
efflorescence of technological and artistic expression in H.
sapiens. Rather than a benchmark for modern human
behaviour, the behavioural expression of these H. sapiens
populations expanding into Europe is atypical of many
other late Pleistocene human records elsewhere (e.g.
Habgood and Franklin 2008; Mackay et al. 2014). We
suggest that interaction between and within frontier popu-
lations may have served as the catalyst for these artistic and
technological developments. A potentially similar process
can be observed in late Pleistocene southern Africa. Pop-
ulations migrating into the region at the advent of the Later
Stone Age may have introduced technological novelties
(Hammer et al. 2011; Pickrell et al. 2012; Villa et al. 2012),
but only with subsequent expansions of interaction zones
do we begin to see the full range of modern behaviours
(Mackay et al. 2014). To phrase that another way, the
modern signature does not flourish in southern Africa with
the initial appearance of the Later Stone Age; it follows the
transmission of genetic and cultural information between
individuals occupying areas previously isolated from one
another.
Previous researchers have argued that there is archaeo-
logical evidence for cultural exchange between archaic
lineages, particularly in Eurasia (e.g. Mellars et al. 2007).
However, what we are suggesting is not merely that culture
was exchanged between archaic hominins over the course
of the Middle to Late Pleistocene, but that contact and the
subsequent exchange of culture could have created an
environment that spurred the type of innovation that has
been identified in the archaeological record as evidence for
emergent modern culture. In this scenario it was contact
itself that facilitated the emergence of aspects of cultural
modernity. Notably, in areas with relative occupational
stability through the late Pleistocene, modernity emerges
gradually (Ambrose 1998), and some ‘archaic’ cultural
characteristics persist until the recent past (Leplongeon
2013).
Challenges in the Study of Hybrid Human Origins
Increasingly evidence points to a complex pattern of
divergence and merger among archaic populations, indi-
cating that the product we see today (extant modern
humans) is the result not of diverging lineages, but of
divergence plus anastomosis. One of the major challenges
for future researchers will be to model what this process
might have looked like, and to interpret the archaeological
and biological patterns we see in the present and past in
light of this model. A starting point would be to move away
from a strictly tree-like metaphor (i.e. branching only) for
evolution and diversification. We suggest that a more
complex metaphor that incorporates frequent hybridization
as a core feature (e.g. a network or braided stream) is a
more apt way to consider the emergence and evolution of
our species. Importantly, gene flow does not only cause
branches to merge, but can also spur the production of new
branches, which themselves can interact with other bran-
ches. Diversification is therefore a product of the interac-
tion of processes (e.g. drift, gene flow, selection) driving
both divergence and merger. Moreover, ancestor-descen-
dent relationships are complex due to the dynamics of
divergence and gene exchange between individuals, pop-
ulations, and species. Reconsidering the diversity we see in
both the fossil and archaeological record in this light could
allow for a more nuanced understanding of the past, but
this will be a challenge to model. Predictions based on
evolutionary theory and analogue organisms (e.g.
baboons), as well as ethnographic accounts, provide one
means for modelling what we might expect both culturally
and biologically when humans come into contact.
Related to this, we need to make a more concerted effort
to bring together the lines of evidence—genetic, pheno-
typic, cultural—to better understand what is undoubtedly a
complex network of exchange with both biological and
cultural effects. To date there has been very limited col-
laboration between researchers investigating these different
aspects of the human organism, and this lack of commu-
nication and understanding has probably played some part
in the divergence of opinion on modern human origins.
Ongoing efforts also need to be made to recover more
genomes from Africa in the deeper past. Almost all whole-
genome comparisons to date are between extant human
genomes and archaic ‘‘non-modern’’ ones (but see e.g. Fu
et al. 2014; Seguin-Orlando et al. 2014), while archaeo-
logical evidence compares individuals at the same place
Evol Biol
123

and time. We still do not understand the true genetic
relationship between ancient (i.e. Later Pleistocene) Afri-
cans and extant people (or ancient Africans and Nean-
derthals), which would better inform and complement the
interpretation of the other lines of evidence.
Prospects and Conclusions
That hybridization has had a profound effect on the evo-
lutionary history of our species is, in our minds, a settled
issue. However, many questions remain. In particular, we
think the following are of paramount importance. First,
how much of the variation that we see in the fossil record
can be explained by gene exchange relative to other factors
influencing diversification (i.e. selection, drift)? These
evolutionary forces are not mutually exclusive, and they
certainly interacted in complex ways to produce the vari-
ation we see in our lineage. Our understanding of the
evolutionary underpinnings of phenotypic variation is
extremely limited and relies heavily on adaptive models.
Second, to what extent are hybridization and contact
responsible for the major phenotypic and cultural changes
we see in the palaeontological and archaeological record?
We proposed here that they play a significant role, but this
needs considerably more investigation to test the subtleties
of this relationship, and to consider it in deeper time. The
little we know suggests that hybridization might be
responsible for increasing variation and complexity within
our lineage, and for the increasing ability of humans to
evolve (e.g. adapt to new contexts). Hybridization could
also have played a major role in driving change at other
points in time, such as at the emergence of our genus
Homo, a period characterised by biological and cultural
innovation, and a diversity of forms (Anto
´n et al. 2014),
though this hypothesis needs further exploration. Finally,
we need to reconsider the basis of taxonomic distinctions
between these various hybridizing groups in light of cur-
rent evidence (‘‘Appendix 2’’); as things stand the termi-
nology of modern human origins provides one more
impediment to our ability to move towards a more nuanced
understanding of the evolutionarily complex origins of our
lineage.
Acknowledgments We would like to thank Charles Roseman and
Dietmar Zinner for their comments that greatly improved this
manuscript. RRA hybrid research supported by Grants from the
National Research Foundation of South Africa and the DST/NRF
Centre of Excellence in Palaeosciences (COE-Pal).
Conflict of interest The authors declare that they have no conflict
of interest.
Appendix 1: Traditional Views (and Our View)
of Modernity
Homo sapiens is the only hominin species alive today; we
consider all humans living today modern. Traditionally,
archaeologists and palaeoanthropologists have defined
modernity in both cultural and biological terms (Fig. 1).
The evidence for biological modernity has come from the
fossil record, and refers to hominins that look (essentially)
like us in terms of their skeletons (e.g. large brains, gracile
postcrania). Fossils considered to be early modern humans
are by no means homogenous, and indeed even the
expression of modern features varies across these speci-
mens (McBrearty and Brooks 2000). The evidence for
cultural modernity derives from archaeological materials
that signal aspects of modern intellectual, symbolic, lin-
guistic and technological capabilities; interpretation of
specific artefacts as modern is not straightforward and
often controversial (e.g. Botha 2008; Klein 2013).
There are multiple views on when and how modern
humanness arose. One view is that while the earliest
modern humans in Africa showed derived morphological
traits that put them on the path to modernity circa 200 ka,
true modernity only arose sometime around 50 ka when an
adaptively beneficial neurological change prompted beha-
vioural innovation, providing Africans with a fitness
advantage over other archaic peoples (e.g. Klein 1995).
Others view the emergence of modernity as more cumu-
lative (e.g. McBrearty and Brooks 2000), occurring over
the course of hundreds of thousands of years or more, again
primarily in Africa. Both of these models are directional.
Regardless, most researchers agree that signatures of cog-
nitive modernity (such as figurative art) only become
commonplace after 50 ka, suggesting that complete cul-
tural and biological modernity are relatively recent
phenomena.
Our view of the emergence of modernity differs in key
respects to those depicted above. We view the emergence
of our lineage as a continuing dynamic (process) rather
than an outcome (product); there is no clear starting point,
or ending point, but rather an ongoing, repeating process of
divergence and hybridization at multiple points in its
evolutionary history. It is the dynamics of this repeated
lineage divergence and remerger that has produced the
variation observable in our genome (and phenome) today.
We would not expect the directional accumulation of
modernity in such a scenario, but rather a sporadic, flick-
ering signal (see also d’Errico and Stringer 2011 for a
similar argument on the early archaeological record of the
human lineage). In this scenario, references to ‘‘moder-
nity’’ or ‘‘archaicness’’ become problematic (see
Evol Biol
123

‘‘Appendix 2’’); we would suggest abandoning the terms in
the context of the origins and evolution of H. sapiens.
Appendix 2: Questions of Taxonomy
Currently the term modern humans, or modern Homo
sapiens, is used almost exclusively in the palaeoanthro-
pological and archaeological literature to refer to people
emerging from Africa—i.e. people of African origin.
However, we now know that Neanderthals and Denisovans
(and potentially other archaic lineages) are part of many
peoples’ ancestry today, raising the question of whether it
is valid to exclude them from our species. Considered
another way, if you send your cheek swab into learn your
ancestry and find out you are 10 % Neanderthal, it would
be nonsense to say that you are 90 % modern human.
Additionally, given the increasing genetic and morpho-
logical evidence for hybridization emerging from the fossil
record, it is likely that the assignment of certain individuals
to current taxonomic categories is impossible. It is almost
certain that individuals previously defined as modern
humans or Neanderthals (or something else) are actually
hybrids, as recently argued on the basis of both genetics
(Fu et al. 2015) and morphology (Ackermann 2010).
Defining Homo sapiens has always been problematic
(see discussion in Wood 2011). Relying on shared derived
characteristics such as big brains and language abilities
does not incontrovertibly exclude groups like Neanderthals
who also had large brains and may have had comparable
cognitive abilities (Vanhaeren et al. 2006; Bouzouggar
et al. 2007; Peresani et al. 2011,2013; Rodrı
´guez-Vidal
et al. 2014). Using a common approach for determining
affinities of fossils—i.e. a phenotype within or close to the
range of humans living today—is also problematic given
that today’s range includes the effects of hybridization, as
discussed here. More pointedly, even traits acquired
through hybridization are ‘modern’ in the sense that they
contribute to the range of variation seen in people living
today. We suggest at this time, and until more is known
about phenotypic and genomic variation in Pleistocene
groups, that considering Homo sapiens as a single complex
lineage, with significant divergence and anastomosis
among sub-groups, is the most inclusive and accurate
approach. We would like to see the elimination of the term
‘modern humans’ in exchange for simply calling our taxon
H. sapiens, with people alive today referred to as living
(extant) humans. We would recommend that researchers
consider everyone prior to living people who contributed
directly to the variation in our lineage as human ancestors
with regional population names like Denisovans and
Europeans, rather than giving them species-level distinc-
tions.. We recommend this last measure because referring
to e.g. Neanderthals versus ‘modern humans’ gives the
incorrect impression that certain human groups living
today are less modern than others.
Were these ancestral groups distinct species? Most
evolutionary biologists would agree that species should be
so-called if they retain morphological, behavioural and
genetic differences even in the face of gene flow (e.g.
Coyne and Orr 2004), and certainly Africans and Nean-
derthals (and potentially others) likely remained divided
over a (relatively) geologically short evolutionary time
period due to geographic barriers, becoming distinct lin-
eages in isolation (or near isolation). Humans living today
represent a genomically coherent species. Whether and
which ancient Homo taxa (including Pleistocene H. sapi-
ens) can be considered monophyletic, genomically coher-
ent species will have to await sequences of numerous
genomes from across the range of their distribution(s).
However, this description of what keeps species distinct
also implies that the ability to coexist geographically
(sympatry) without the fusion of lineages is a result of
being separate species (Mallet 2008). It is less clear whe-
ther this was the case. Indeed, post-contact gene flow and
the subsequent disappearance of all but a single lineage
suggests that these archaic lineages may not have been able
to coexist without the fusion of lineages.
Fig. 1 Representative fossil and archaeological evidence tradition-
ally used to indicate biological and cultural modernity. From left to
right A modern human mandible from Klasies River, South Africa;
perforated shell beads and incised ochre from Blombos, South Africa;
bone harpoon from Katanda, Democratic Republic of Congo [images
not to scale] (Illustration: TA Sumner)
Evol Biol
123

References
Abi-Rached, L., Jobin, M. J., Kulkarni, S., McWhinnie, A., Dalva, K.,
Gragert, L., et al. (2011). The shaping of modern human immune
systems by multiregional admixture with archaic humans.
Science, 334(6052), 89–94.
Ackermann, R. R. (2010). Phenotypic traits of primate hybrids:
Recognizing admixture in the fossil record. Evolutionary
Anthropology, 19, 258–270.
Ackermann, R. R., Rogers, J., & Cheverud, J. (2006). Identifying the
morphological signatures of hybridization in primate and human
evolution. Journal of Human Evolution, 51, 632–645.
Ackermann, R. R., Schroeder, L., Rogers, J., & Cheverud, J. (2014).
Further evidence for phenotypic signatures of hybridization in
descendant baboon populations. Journal of Human Evolution,
74, 54–62.
Glossary
Accretion Model A model of modern human origins that
proposes an African origin for
biologically modern humans, but
includes a small but significant amount
of admixture (*10 %) between these
groups and local populations upon
leaving Africa and spreading across
Eurasia (Smith 2010).
Acheulean A technological industry associated with
the production of large cutting tools,
such as handaxes and cleavers. The
Acheulean has a vast temporal and
spatial spread, persisting from
*1.75 Ma to \500 ka (Herries 2011),
and extending from Africa through
Europe to west Asia. The presence of
an Acheulean in east Asia is the
subject of ongoing debate.
Admixture The production of new genetic
combinations in hybridizing groups.
Afro-European sapiens
Hypothesis
A version of modern human origins that
favours a gradual, mosaic-like process
of anatomical modernization in Africa
over approximately a half million years.
Accepts possibility of very minimal
evidence for interbreeding outside of
Africa (e.g. with Neanderthals) as
African people migrated to the rest of
the world (Bra
¨uer 2008).
Denisovans A recently discovered group of
genetically distinct hominins known
from a handful of bones and teeth, who
lived 41 kya in Siberia. DNA analyses
have shown that they share a common
ancestor with Neanderthals, and
contributed to the genetic make-up of
some Oceanic populations (Krause
et al. 2010; Reich et al. 2011).
Hominin Thecolloquial termfor members of the tribe
Hominini. This tribe includes humans, as
well as all of our extinct ancestors that
evolved after the split from the tribe
Panini (chimpanzees and bonobos).
Gene Flow The transfer of genes (DNA) from one
population to another.
Hybridization (Natural
Hybridization)
Successful matings (in nature) between
individuals from genetically
differentiated lineages.
Introgressive
Hybridization, or
Introgression
The transfer of DNA between
individuals from two genetically
differentiated lineages via
hybridization, followed by repeated
backcrossing between hybrid and
parental individuals and the subsequent
movement of genes back into parental
population(s). This can be
unidirectional or bidirectional.
Glossary
Later Stone Age The period following the Middle Stone Age in
Africa, and often seen to parallel the Upper
Palaeolithic in Europe, the Later Stone Age is
viewed by many researchers as reflecting the
appearance of fully modern behaviour in the
archaeological record. Art, symbolism and
ornamentation become entrenched in the Later
Stone Age after episodic expression in the
Middle Stone Age. The advent of the Later Stone
Age is spatially and temporally complex, with
earliest dates ranging from[46 ka in east Africa
to\22 ka in parts of southern Africa (Opperman
and Heydenrych 1990; Ambrose 1998).
Levant An area of south west Asia that lies between
Africa and Europe, the Levant records the
fluctuating range extensions of Eurasian and
African fauna—including Neanderthals and
African-derived modern humans—through the
Middle and Late Pleistocene (Tchernov 1994).
Mousterian A technological industry originally associated
with Neanderthals in Europe and featuring a
diversity of forms linked by use of the
Levallois core reduction concept (Boe
¨da
1995). Middle Stone Age industries in North
Africa are sometimes also referred to as
‘Mousterian’, though clear Neanderthal
remains are absent in the region.
Neanderthals A taxon of hominins that lived in Eurasia from
approximately *250–40 ka. Neanderthals are
known to differ both morphologically and
culturally from their African counterparts,
being physically robust and having a well-
established stone tool tradition, the Mousterian.
Pleistocene A geological epoch dated from approximately
2.588 million to 11,700 years before present
(BP). Humans evolved into their present form
during this time.
Transgressive
Phenotypes
Phenotypes in hybrids that exceed the range of
phenotypes that are observed in the parental
taxa (Seehausen et al. 2014).
Evol Biol
123

Ahern, J., Jankovic, I., Voison, J.-L., & Smith, F. (2013). Modern
human origins in central Europe. In F. H. Smith & J. Ahern
(Eds.), Origins of modern humans: Biology reconsidered (2nd
ed., pp. 151–222). London: Wiley.
Ambrose, S. H. (1998). Chronology of the Later Stone Age and food
production in East Africa. Journal of Archaeological Science,
25, 377–392.
Anto
´n, S., Richard, P., & Aiello, L. C. (2014). Evolution of early
Homo: An integrated biological perspective. Science, 345(6192),
1236828.
Arnold, M. L. (1992). Natural hybridization as an evolutionary
process. Annual Reviews of Ecology and Systematics, 23,
237–261.
Arnold, M., & Meyer, A. (2006). Natural hybridization in primates:
One evolutionary mechanism. Zoology, 109, 261–276.
Bar-Yosef Mayer, D. E., Vandermeersch, B., & Bar-Yosef, O. (2009).
Shells and ochre in Middle Paleolithic Qafzeh Cave, Israel:
Indications for modern behavior. Journal of Human Evolution,
56(3), 307–314.
Boe
¨da, E. (1995). Levallois: A volumetric construction, methods, a
technique. In H. L. Dibble & O. Bar-Yosef (Eds.), The definition
and interpretation of Levallois Technology (pp. 41–68).
Madison, WI: Prehistory Press.
Botha, R. (2008). Prehistoric shell beads as a window on language
evolution. Language and Communication, 28(3), 197–212.
Bouzouggar, A., Barton, N., Vanhaeren, M., d’Errico, F., Collcutt, S.,
Higham, T., et al. (2007). 82,000-Year-old shell beads from
North Africa and implications for the origins of modern human
behavior. Proceedings of the National Academy of Sciences of
the United States of America, 104(24), 9964–9969.
Brau
¨er, G. (1981). New evidence on the transitional period between
Neanderthal and modern man. Journal of Human Evolution, 10,
467–474.
Brau
¨er, G. (1985). The ‘‘Afro-European sapiens-hypothesis’’ and
hominid evolution in East Asia during the late Middle and Upper
Pleistocene. Courier Forsch Senckenberg, 69, 145–165.
Bra
¨uer, G. (2008). The origin of modern anatomy: By speciation or
intraspecific evolution? Evolutionary Anthropology: Issues,
News, and Reviews, 17(1), 22–37.
Callaway, E. (2015). Neanderthals had outsize effect on human
biology. Nature, 523, 512–513.
Cohen, R. (2007). Creolization and cultural globalization: The soft
sounds of fugitive power. Globalizations, 4(2), 1–25.
Condemi, S., Mounier, A., Giunti, P., Lari, M., Caramelli, D., &
Longo, L. (2013). Possible interbreeding in late Italian Nean-
derthals? New data from the Mezzena Jaw (Monti Lessini,
Verona, Italy). PLoS One, 8, 1–9.
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA:
Sinauer Associates.
Curnoe,D.,Ji,X.,Tac¸on, P. S. C., & Yaozheng, G. (2015). Possible
signatures of hominin hybridization from the early Holocene of
southwest China. Scientific Reports, 5, 12408. doi:10.1038/srep12408.
Dannemann, M., Andre
´s, A. M., & Kelso, J. (2015). Adaptive variation
in human toll-like receptors is contributed by introgression from
both Neandertals and Denisovans. doi:10.1101/022699.
d’Errico, F., & Stringer, C. B. (2011). Evolution, revolution or
saltation scenario for the emergence of modern cultures?
Philosophical Transactions of the Royal Society of London.
Series B, Biological Sciences, 366(1567), 1060–1069.
Ding, Q., Hu, Y., Xu, S., Wang, J., & Jin, L. (2014). Neanderthal
introgression at chromosome 3p21.31 was under positive natural
selection in East Asians. Molecular Biology and Evolution, 31,
683–695.
Dowling, T. E., & Secor, C. L. (1997). The role of hybridization in the
evolutionary diversification of animals. Annual Review of
Ecology, Evolution and Systematics, 28, 593–619.
Duarte, C., Maurı
´cio, J., Pettitt, P. B., Souto, P., Trinkaus, E., van der
Plicht, H., et al. (1999). The early Upper Paleolithic human
skeleton from the Abrigo do Lagar Velho (Portugal) and modern
human emergence in Iberia. Proceedings of the National
Academy of Sciences of the United States of America, 96,
7604–7609.
Fu, Q., Hajdinjak, M., Moldovan, O. T., Constantin, S., Mallick, S.,
Skoglund, P., et al. (2015). An early modern human from
Romania with a recent Neanderthal ancestor. Nature,524,
216–219.
Fu, Q., Li, H., Moorjani, P., Jay, F., Slepchenko, S. M., Bondarev, A.
A., et al. (2014). Genome sequence of a 45,000-year-old modern
human from western Siberia. Nature, 514(7523), 445–449.
Fu, Q., Meyer, M., Gao, X., Stenzel, U., Burbano, H. A., Kelso, J.,
et al. (2013). DNA analysis of an early modern human from
Tianyuan Cave, China. Proceedings of the National Academy of
Sciences of the Unites States of America, 110, 2223–2227.
Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U.,
Kircher, M., et al. (2010). A draft sequence of the Neandertal
genome. Science, 328(5879), 710–722.
Habgood, P. J., & Franklin, N. R. (2008). The revolution that didn’t
arrive: A review of Pleistocene Sahul. Journal of Human
Evolution, 55(2), 187–222.
Hammer, M. F., Woerner, A. E., Mendez, F. L., Watkins, J. C., &
Wall, J. D. (2011). Genetic evidence for archaic admixture in
Africa. Proceedings of the National Academy of Sciences,
108(37), 15123–15128.
Harrison, R. (1986). Pattern and process in a narrow hybrid zone.
Heredity, 56, 337–349.
Herries, A. I. (2011). A chronological perspective on the Acheulian
and its transition to the Middle Stone Age in southern Africa:
The question of the Fauresmith. International Journal of
Evolutionary Biology, 2011, 961401.
Higham, T., Douka, K., Wood, R., Bronk Ramsey, C., Brock, F.,
Basell, L., et al. (2014). The timing and spatiotemporal
patterning of Neanderthal disappearance. Nature, 512,
306–309.
Hublin, J.-J., Talamo, S., Julien, M., David, F., Connet, N., Bodu, P.,
et al. (2012). Radiocarbon dates from the Grotte du Renne and
Saint-Ce
´saire support a Neandertal origin for the Cha
ˆtelperro-
nian. Proceedings of the National Academy of Sciences, 109(46),
18743–18748.
Huerta-Sa
´nchez, E., Jin, X., Asan, B. Z., Peter, B., Vinckenbosch, N.,
et al. (2014). Altitude adaptation in Tibetans caused by
introgression of Denisovan-like DNA. Nature, 512, 194–197.
Joordens, J. C. A., d’Errico, F., Wesselingh, F. P., Munro, S., de Vos,
J., Wallinga, J., et al. (2015). Homo erectus at Trinil on Java
used shells for tool production and engraving. Nature,
518(7538), 228–231.
Key, K. (1968). The concept of stasipatric speciation. Systematic
Zoology, 17, 14–22.
Key, F. M., Teixeira, J. C., de Filippo, C., & Andre
´s, A. M. (2014).
Advantageous diversity maintained by balancing selection in
humans. Current Opinion in Genetics and Development, 29, 45–51.
Klein, R. G. (1995). Anatomy, behaviour and modern human origins.
Journal of World Prehistory, 9, 167–198.
Klein, R. G. (2013). Modern human origins. General Anthropology,
20(1), 1–4.
Krause, J., Fu, Q., Good, J. M., Viola, B., Shunkov, M. V.,
Derevianko, A. P., & Paabo, S. (2010). The complete mitochon-
drial DNA genome of an unknown hominin from southern
Siberia. Nature, 464(7290), 894–897.
Lachance, J., Vernot, B., Elbers Clara, C., Ferwerda, B., Froment, A.,
Bodo, J.-M., et al. (2012). Evolutionary history and adaptation
from high-coverage whole-genome sequences of diverse African
hunter-gatherers. Cell, 150(3), 457–469.
Evol Biol
123

Leplongeon, A. (2013). Microliths in the Middle and Later Stone Age
of eastern Africa: New data from Porc-Epic and Goda Buticha
cave sites, Ethiopia. Quaternary International,343, 100–116.
Lightfoot, K. G., & Martinez, A. (1995). Frontiers and boundaries in
archaeological perspective. Annual Review of Anthropology, 24,
471–492.
Mackay, A., Stewart, B. A., & Chase, B. M. (2014). Coalescence and
fragmentation in the late Pleistocene archaeology of southern-
most Africa. Journal of Human Evolution, 72, 26–51.
Mallet, J. (2005). Hybridization as an invasion of the genome. Trends
in Ecology and Evolution, 20, 229–237.
Mallet, J. (2008). Hybridization, ecological races and the nature of
species: empirical evidence for the ease of speciation. Philo-
sophical Transactions of the Royal Society B, 363, 2971–2986.
McBrearty, S., & Brooks, A. S. (2000). The revolution that wasn’t: a
new interpretation of the origin of modern human behavior.
Journal of Human Evolution, 39(5), 453–563.
McDougall, I., Brown, F. H., & Fleagle, J. G. (2005). Stratigraphic
placement and age of modern humans from Kibish, Ethiopia.
Nature, 433(7027), 733–736.
McElreath, R., Boyd, R., & Richerson, P. J. (2003). Shared norms and
the evolution of ethnic markers. Current Anthropology, 44(1),
122–130.
Mellars, P., Gravina, B., & Bronk Ramsey, C. (2007). Confirmation
of Neanderthal/modern human interstratification at the
Chatelperronian type-site. Proceedings of the National Academy
of Sciences, 104(9), 3657–3662.
Meyer, M., Fu, Q., Aximu-Petri, A., Glocke, I., Nickel, B., Arsuaga,
J.-L., et al. (2014). A mitochondrial genome sequence of a
hominin from Sima de los Huesos. Nature, 505, 403–406.
Meyer, M., Kircher, M., Gansauge, M.-T., Li, H., Racimo, F.,
Mallick, S., et al. (2012). A high-coverage genome sequence
from an archaic Denisovan individual. Science, 338, 222–226.
Nosil, P., & Feder, J. L. (2012). Widespread yet heterogeneous
genomic divergence. Molecular Ecology, 21, 2829–2832.
Opperman, H., & Heydenrych, B. (1990). A 22,000-year old Middle
Stone Age camp site with plant food remains from the north-
eastern Cape. South African Archaeological Bulletin, 45, 93–99.
Pearson, O. M. (2013). Hominin evolution in the middle-late
pleistocene: Fossils, adaptive scenarios, and alternatives. Cur-
rent Anthropology, 54(S8), S221–S233.
Peresani, M., Fiore, I., Gala, M., Romandini, M., & Tagliacozzo, A.
(2011). Late Neanderthals and the intentional removal of
feathers as evidenced from bird bone taphonomy at Fumane
Cave 44 ky B.P., Italy. Proceedings of the National Academy of
Sciences, 108(10), 3888–3893.
Peresani, M., Vanhaeren, M., Quaggiotoo, E., Queffelec, A., &
d’Errico, F. (2013). An Ochered fossil marine shell from the
Mousterian of Fumane Cave, Italy. PLoS One, 8(7), e68572.
Pickrell, J. K., Patterson, N., Barbieri, C., Berthold, F., Gerlach, L.,
Guldemann, T., et al. (2012). The genetic prehistory of southern
Africa. Nature Communications, 3, 1143.
Prufer, K., Racimo, F., Patterson, N., Jay, F., Sankararaman, S.,
Sawyer, S., et al. (2014). The complete genome sequence of a
Neanderthal from the Altai Mountains. Nature, 505(7481),
43–49.
Ramirez Rozzi, F., d’Errico, F., Vanhaeren, M., Grootes, P.,
Kerautret, B., & Dujardin, V. (2009). Cutmarked human remains
bearing Neanderthal features and modern human remains
associated with the Aurignacian at Les Rois. Journal of
Anthropological Sciences, 87, 153–185.
Reich, D., Patterson, N., Kircher, M., Delfin, F., Nandineni
Madhusudan, R., Pugach, I., et al. (2011). Denisova admixture
and the first modern human dispersals into southeast Asia and
Oceania. The American Journal of Human Genetics, 89(4),
516–528.
Rightmire, G. P. (2009). Middle and later Pleistocene hominins in
Africa and Southwest Asia. Proceedings of the National
Academy of Sciences, 106(38), 16046–16050.
Rodrı
´guez-Vidal, J., d’Errico, F., Pacheco, F. G., Blasco, R., Rosell,
J., Jennings, R. P., et al. (2014). A rock engraving made by
Neanderthals in Gibraltar. Proceedings of the National Academy
of Sciences, 111(37), 13301–13306.
Rougier, H., Milota, S¸ ., Rodrigo, R., Gherase, M., Sarcina
ˇ, L.,
Moldovan, O., et al. (2007). Pes¸tera cu Oase 2 and the cranial
morphology of early modern Europeans. Proceedings of the
National Academy of Sciences, 104(4), 1165–1170.
Sadr, K. (2003). The Neolithic of Southern Africa. Journal of African
History, 44(2), 195–209.
Sankararaman, S., Mallick, S., Dannemann, M., Prufer, K., Kelso,
J., Paabo, S., et al. (2014). The genomic landscape of
Neanderthal ancestry in present-day humans. Nature,
507(7492), 354–357.
Sankararaman, S., Patterson, N., Li, H., Pa
¨a
¨bo, S., & Reich, D.
(2012). The date of interbreeding between Neandertals and
modern humans. PLoS Genetics, 8(10), e1002947.
Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in
Ecology and Evolution, 19, 198–207.
Seehausen, O., Butlin, R., Keller, I., Wagner, C., Boughman, J.,
Hohenlohe, P., et al. (2014). Genomics and the origin of species.
Nature Reviews Genetics, 15, 176–192.
Seguin-Orlando, A., Korneliussen, T. S., Sikora, M., Malaspinas, A.-
S., Manica, A., Moltke, I., et al. (2014). Genomic structure in
Europeans dating back at least 36,200 years. Science,346(6213),
1113–1118.
Se
´gurel, L., & Quintana-Murci, L. (2014). Preserving immune
diversity through ancient inheritance and admixture. Current
Opinion in Immunology, 30, 79–84.
Slatkin, M. (1985). Gene flow in natural populations. Annual Review
of Ecology and Systematics, 16, 393–430.
Smith, F. H. (2010). Species, populations, and assimilation in later
human evolution. In C. S. Larsen (Ed.), A companion to
biological anthropology (pp. 357–378). Oxford: Wiley-
Blackwell.
Smith, F. H. (2013). The fate of the Neandertals. Journal of
Anthropological Research, 69, 167–200.
Soficaru, A., Petrea, C., Dobos, A., & Trinkaus, E. (2006). Early
modern humans from the Pestera Muierii, Baia de Fier,
Romania. Proceedings of the National Academy of Sciences of
the United States of America, 103(46), 17196–17201.
Tchernov, E. (1994). New comments on the biostratigraphy of the
Middle and Upper Pleistocene of the southern Levant. In O. Bar-
Yosef & R. S. Kra (Eds.), Late quaternary chronology and
paleoclimates of the eastern Mediterranean (pp. 333–350).
Tucson: Radiocarbon.
Trinkaus, E. (2007). European early modern humans and the fate of
the Neanderthals. Proceedings of the National Academy of
Sciences, 104, 7367–7372.
Trinkaus, E. (2013). Life and Death at the Pestera cu Oase. A Setting
for Modern Human Emergence in Europe. Oxford: Oxford
University Press.
Vanhaeren, M., D’Errico, F., Stringer, C., James, S. L., Todd, J. A., &
Mienis, H. K. (2006). Middle Paleolithic shell beads in Israel and
Algeria. Science, 312, 1785–1788.
Veeramah, K. R., & Hammer, M. F. (2014). The impact of whole-
genome sequencing on the reconstruction of human population
history. Nature Reviews Genetics, 15(3), 149–162.
Vernot, B., & Akey, J. M. (2014). Resurrecting surviving Neandertal
lineages from modern human genomes. Science, 343(6174),
1017–1021.
Villa, P., Soriano, S., Tsanova, T., Degano, I., Higham, T. F. G.,
d’Errico, F., et al. (2012). Border cave and the beginning of the
Evol Biol
123

Later Stone Age in South Africa. Proceedings of the National
Academy of Sciences, 109(33), 13208–13213.
Weaver, T. D., Roseman, C. C., & Stringer, C. B. (2007). Were
neandertal and modern human cranial differences produced by
natural selection or genetic drift? Journal of Human Evolution,
53(2), 135–145.
Wolpoff, M., Hawks, J., Frayer, D., & Hunley, K. (2001). Modern
human ancestry at the peripheries: A test of the replacement
theory. Science, 291(5502), 293–297.
Wood, B. (Ed.). (2011). Homo sapiens Linnaeus, 1758. In Wiley-
Blackwell encyclopedia of human evolution (pp. 332–333).
Oxford: Wiley-Blackwell.
Wu, C.-I. (2001). The genic view of the process of speciation. Journal
of Evolutionary Biology, 14, 851–865.
Wu, X.-J., Xing, S., & Trinkaus, E. (2013). An enlarged parietal
foramen in the Late Archaic Xujiayao 11 neurocranium from
northern China, and rare anomalies among Pleistocene Homo.
PLoS One, 8(3), e59587.
Evol Biol
123