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The Hybrid Origin of “Modern” Humans


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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.
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The Hybrid Origin of ‘‘Modern’’ Humans
Rebecca Rogers Ackermann
Alex Mackay
Michael L. Arnold
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
Department of Archaeology, University of Cape Town,
Rondebosch, South Africa
Centre for Archaeological Science, University of
Wollongong, Wollongong, Australia
Department of Genetics, University of Georgia, Athens, GA,
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
(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
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
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.
¨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
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
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
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
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
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
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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
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
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
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‘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
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)
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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
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
Successful matings (in nature) between
individuals from genetically
differentiated lineages.
Hybridization, or
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.
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
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.
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... Taking this a step further, a number of researchers have suggested that behavioral modernity was also present in pre-modern groups, including outside of Africa, and that this presence and emergence reflects a polycentric origin for behavioral modernity (Conard, 2005;d'Errico, 2003;d'Errico and Stringer, 2011). Building on this, another model that has been put forward by Ackermann et al. (2016) suggests that hybridization and repeated contact between populations was important for the emergence of technological innovation, and that some of the behaviors associated with behavioral modernity could have been due to these interactions. While these competing models have reached different conclusions based on the fossil and archaeological record, there are a number of significant finds from South Africa that have played a large role in these narratives. ...
... Within the framework of these proposed models, the debate about the relative importance of hybridization and resultant introgression has been ongoing since the 1980's (e.g., Ackermann et al., 2016;Smith, 1985;Smith et al., 1989). While new fossil and genetic evidence have exposed a higher frequency of hybridization events than was previously believed, providing a more detailed picture of the complexity of our origins (e.g., Villanea and Schraiber, 2019), the idea that hybridization played a significant role during the evolution of H. sapiens is not new. ...
... The "Assimilation model", first proposed by Smith (1985), argues that gene flow and admixture between migrating modern humans out of Africa and premodern Eurasians was an important driver and contributor to the morphological change that led to the emergence of humans. This model has also been expanded into the "Divergence and Hybridization" model (Ackermann et al., 2016), which views the origin of humans as a continuous process of genetic and cultural exchange between groups (all of whom are recognized as human ancestors), both inside and out of Africa, resulting in both morphological diversity and cultural innovation, a precursor to the variability that we see today. This model depicts multiple origins across time and space, instead of a single population evolving in a single place at a certain time. ...
... In addition to phenotypic evidence, we also have considerabledand ever-growingdgenetic evidence for hybridization between post-1 Ma lineages in human evolution, the period relevant to the origin of our species, H. sapiens. This genetic evidence has been well-described elsewhere (e.g., Ackermann et al., 2016;Dannemann and Racimo, 2018;Ackermann et al., 2019;Gokcumen, 2020), and includes evidence for movement of gene variants from Neanderthals into early humans (Green et al., 2010;Fu et al., 2014Fu et al., , 2015Villanea and Schraiber, 2019;Hajdinjak et al., 2021;Prüfer et al., 2021), and vice versa (Kuhlwilm et al., 2016;Posth et al., 2017;Chen et al., 2020), from Denisovans into early humans (Reich et al., 2010;Meyer et al., 2012), and from both Neanderthals Slon et al., 2018) and some unknown hominin into Denisovans. It also includes evidence for a first-generation child of a Neanderthal mother and a Denisovan father (Slon et al., 2018), and for genetic exchanges between ancient and recent lineages in Africa (Hammer et al., 2011;Lachance et al., 2012;Chen et al., 2020;Durvasula and Sankararaman, 2020;Lipson et al., 2020;Wang et al., 2020). ...
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The Journal of Human Evolution (JHE) was founded 50 years ago when much of the foundation for how we think about human evolution was in place or being put in place, providing the main framework for how we consider our origins today. Here, we will explore historical developments, including early JHE outputs, as they relate to our understanding of the relationship between phenotypic variation and evolutionary process, and use that as a springboard for considering our current understanding of these links as applied to human evolution. We will focus specifically on how the study of variation itself has shifted us away from taxonomic and adaptationist perspectives toward a richer understanding of the processes shaping human evolutionary history, using literature searches and specific test cases to highlight this. We argue that natural selection, gene exchange, genetic drift, and mutation should not be considered individually when considering the production of hominin diversity. In this context, we offer suggestions for future research directions and reflect on this more complex understanding of human evolution and its broader relevance to society. Finally, we end by considering authorship demographics and practices in the last 50 years within JHE and how a shift in these demographics has the potential to reshape the science of human evolution going forward.
... If this represents a problem, obviously it is a lot bigger than anthropology. Indeed, many researchers in bioanthropology today are even reconsidering our favourite metaphor aloud and discussing human ancestry as not so much a Darwinian tree, but as a decidedly non-Darwinian braided stream (Ackermann et al. 2016) or metapopulation (Scerri et al. 2019). ...
We posit that it is trite to compare equids with Pecora or ruminants and conclude that the equid lifestyle is less ‘successful’ because equids are hindgut-fermenters and happen to be less speciose than ruminants. Indeed, ‘speciosity’ is a poorly supported attribute of ‘success’ which itself is poorly defined. Yet, it appears that the current number of equid species is smaller than it was when Equus, and its allied genera, still naturally occurred in the Americas in the Late Miocene and Pliocene. On the other hand, a much-needed revision of the genus, based on genetics, may show a number of ‘hidden species’ that are bundled within the kulans and the Burchell’s zebra. Besides speciosity, geographic extent of a species or a group of species is often also used to indicate ‘successfulness’. If that criterion is applied to the Modern genus, after it expanded into Eurasia and Africa (but before humans started hemming it in and competing for land), as compared to before it left the Americas behind, then the startling conclusion is that Equus became more ‘successful’. Many ‘theories’ and ‘hypotheses’ that have been formulated to ‘explain’ the morphological features of equids can safely be rejected based on new research that is presented here. And so can the notion that equids are somehow inferior to bovids and other Pecora: on the contrary, equids are marvellously well adapted.
The phylogenetic relationships between fossil hominin taxa have been a contentious topic for decades. Recent discoveries of new taxa, rather than resolving the issue, have only further confused it. Compounding this problem are the limitations of some of the tools frequently used by paleoanthropologists to analyze these relationships. Most commonly, phylogenetic questions are investigated using analytical methods such as maximum parsimony and Bayesian analysis. While these are useful analytical tools, these tree-building methods can have limitations when investigating taxa that may have complex evolutionary histories. Exploratory data analysis can provide information about patterns in a dataset that are obscured by tree-based methods. These patterns include phylogenetic signal conflict, which is not depicted in tree-based methods. Signal conflict can have a number of sources, including methodological issues with character choice, taxonomic issues, homoplasy, and gene flow between taxa. In this study, an exploratory data analysis of fossil hominin morphological data is conducted using the tree-based analytical method neighbor-joining and the network-based analytical method neighbor-net with the goal of visualizing phylogenetic signal conflict within a hominin morphological data set. The data set is divided into cranial regions, and each cranial region is analyzed individually to investigate which regions of the skull contain the highest levels of signal conflict. Results of this analysis show that conflicting phylogenetic signals are present in the hominin fossil record during the relatively speciose period between 3 and 1 Ma, and they also indicate that levels of signal conflict vary by cranial region. Possible sources of these conflicting signals are then explored. Exploratory data analyses such as this can be a useful tool in generating phylogenetic hypotheses and in refining character choice. This study also highlights the value network-based approaches can bring to the hominin phylogenetic analysis toolkit.
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The high degree of biosocial complexity of the human skull is due not only to the numerous elements that make up this region, but also to the different parts being shaped by both biological processes and ecological factors during development, as well as the individuals’ agency, and their social and cultural environment. Different modules of the skull have specific developmental and embryological origins by which they acquire their final adult shape. As a result, those elements that finish their growth later in life will be more subjected to environmental influences and behaviour than those that acquire the adult form at an earlier developmental stage, with the latter preserving a stronger signal of population and evolutionary history as a result. But even after development finishes, the skull is still influenced by environmental and cultural factors (i.e. behaviour) throughout an individual’s life. Thus some practices that are triggered by either an individual’s agency and/or their social environment during childhood and adulthood could produce changes in the skull. On top of that, some bones are associated with, and thus influenced by, multiple functions (e.g. the maxillae, which form the upper jaw, the floor of the eye sockets, and the lower sections and sides of the nasal cavity), some functions are shared by several bones (e.g. the maxillae, parietals, and mandible are linked to mastication) while others, such as hearing, are unique to particular bones (e.g. the ear ossicles, temporal bone). Overall, the skull is a mosaic that represents the complex interactions of biological processes and behavioural factors shaping our evolutionary history (see Table 3.1 for a summary of key studies exploring these factors), as well as the particular history of that individual. As a consequence, when studying the human skull, it is necessary to consider the multiple spectra of interacting factors, either when analysing differences between and among taxa, populations, ontogenetic series, or an assemblage of individuals from a shared burial or single palaeontological context.
Since the discovery of a human mandible in 1887 near the present-day city of Banyoles, northeastern Spain, researchers have generally emphasized its archaic features, including the lack of chin structures, and suggested affinities with the Neandertals or European Middle Pleistocene (Chibanian) specimens. Uranium-series and electron spin resonance dating suggest the mandible dates to the Late Pleistocene (Tarantian), approximately ca. 45–66 ka. In this study, we reassessed the taxonomic affinities of the Banyoles mandible by comparing it to samples of Middle Pleistocene fossils from Africa and Europe, Neandertals, Early and Upper Paleolithic modern humans, and recent modern humans. We evaluated the frequencies and expressions of morphological features and performed a three-dimensional geometric morphometric analysis on a virtual reconstruction of Banyoles to capture overall mandibular shape. Our results revealed no derived Neandertal morphological features in Banyoles. While a principal component analysis based on Euclidean distances from the first two principal components clearly grouped Banyoles with both fossil and recent Homo sapiens individuals, an analysis of the Procrustes residuals demonstrated that Banyoles did not fit into any of the comparative groups. The lack of Neandertal features in Banyoles is surprising considering its Late Pleistocene age. A consideration of the Middle Pleistocene fossil record in Europe and southwest Asia suggests that Banyoles is unlikely to represent a late-surviving Middle Pleistocene population. The lack of chin structures also complicates an assignment to H. sapiens, although early fossil H. sapiens do show somewhat variable development of the chin structures. Thus, Banyoles represents a non-Neandertal Late Pleistocene European individual and highlights the continuing signal of diversity in the hominin fossil record. The present situation makes Banyoles a prime candidate for ancient DNA or proteomic analyses, which may shed additional light on its taxonomic affinities.
During the last decade, we have witnessed a significant increase in human fossils whose analysis has forced us to redefine the evolutionary landscape of the genus Homo. The findings of the last 10 years have complicated and enriched our interpretation of the “human bush” by highlighting (1) the great morphological variability of the fossil record during the Pleistocene and (2) a greater role of the Asian continent in the reconstruction of our origin. This article presents a general review of the human fossils found or reanalyzed in the last decade and whose study has caused a change in the current paradigm in human evolution. Our analysis forces us to reconsider many of the basic premises of models such as “Out of Africa 1” and “Out of Africa 2,” especially those that explain human evolution and hominin dispersals as unidirectional, linear, and demographically simple processes. Our review emphasizes the role that Asia plays in the reconstruction of our origin during the Pleistocene, including critical stages for the emergence of our own species.KeywordsNeanderthalDenisovanPaleogenomicsPaleoproteomicsOut of Africa
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Pathogens and the diseases they cause have been among the most important selective forces experienced by humans during their evolutionary history. Although adaptive alleles generally arise by mutation, introgression can also be a valuable source of beneficial alleles. Archaic humans, who lived in Europe and Western Asia for over 200,000 years, were likely well-adapted to the environment and its local pathogens, and it is therefore conceivable that modern humans entering Europe and Western Asia who admixed with them obtained a substantial immune advantage from the introgression of archaic alleles. Here we document a cluster of three toll-like receptors (TLR6-TLR1-TLR10) in modern humans that carries three distinct archaic haplotypes, indicating repeated introgression from archaic humans. Two of these haplotypes are most similar to Neandertal genome, while the third haplotype is most similar to the Denisovan genome. The toll-like receptors are key components of innate immunity and provide an important first line of immune defense against bacteria, fungi and parasites. The unusually high allele frequencies and unexpected levels of population differentiation indicate that there has been local positive selection on multiple haplotypes at this locus. We show that the introgressed alleles have clear functional effects in modern humans; archaic-like alleles underlie differences in the expression of the TLR genes and are associated with reduced microbial resistance and increased allergic disease in large cohorts. This provides strong evidence for recurrent adaptive introgression at the TLR6-TLR1-TLR10 locus, resulting in differences in disease phenotypes in modern humans.
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The transition from the Middle Stone Age (MSA) to the Later Stone Age (LSA) in South Africa was not associated with the appearance of anatomically modern humans and the extinction of Neandertals, as in the Middle to Upper Paleolithic transition in Western Europe. It has therefore attracted less attention, yet it provides insights into patterns of technological evolution not associated with a new hominin. Data from Border Cave (KwaZulu-Natal) show a strong pattern of technological change at approximately 44-42 ka cal BP, marked by adoption of techniques and materials that were present but scarcely used in the previous MSA, and some novelties. The agent of change was neither a revolution nor the advent of a new species of human. Although most evident in personal ornaments and symbolic markings, the change from one way of living to another was not restricted to aesthetics. Our analysis shows that: (i) at Border Cave two assemblages, dated to 45-49 and >49 ka, show a gradual abandonment of the technology and tool types of the post-Howiesons Poort period and can be considered transitional industries; (ii) the 44-42 ka cal BP assemblages are based on an expedient technology dominated by bipolar knapping, with microliths hafted with pitch from Podocarpus bark, worked suid tusks, ostrich eggshell beads, bone arrowheads, engraved bones, bored stones, and digging sticks; (iii) these assemblages mark the beginning of the LSA in South Africa; (iv) the LSA emerged by internal evolution; and (v) the process of change began sometime after 56 ka.
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We have previously described hominin remains with numerous archaic traits from two localities (Maludong and Longlin Cave) in Southwest China dating to the Pleistocene-Holocene transition. If correct, this finding has important implications for understanding the late phases of human evolution. Alternative interpretations have suggested these fossils instead fit within the normal range of variation for early modern humans in East Asia. Here we test this proposition, consider the role of size-shape scaling, and more broadly assess the affinities of the Longlin 1 (LL1) cranium by comparing it to modern human and archaic hominin crania. The shape of LL1 is found to be highly unusual, but on balance shows strongest affinities to early modern humans, lacking obvious similarities to early East Asians specifically. We conclude that a scenario of hybridization with archaic hominins best explains the highly unusual morphology of LL1, possibly even occurring as late as the early Holocene.
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Neanderthals are thought to have disappeared in Europe approximately 39,000-41,000 years ago but they have contributed 1-3% of the DNA of present-day people in Eurasia. Here we analyse DNA from a 37,000-42,000-year-old modern human from Peştera cu Oase, Romania. Although the specimen contains small amounts of human DNA, we use an enrichment strategy to isolate sites that are informative about its relationship to Neanderthals and present-day humans. We find that on the order of 6-9% of the genome of the Oase individual is derived from Neanderthals, more than any other modern human sequenced to date. Three chromosomal segments of Neanderthal ancestry are over 50 centimorgans in size, indicating that this individual had a Neanderthal ancestor as recently as four to six generations back. However, the Oase individual does not share more alleles with later Europeans than with East Asians, suggesting that the Oase population did not contribute substantially to later humans in Europe.
From skin disorders to the immune system, sex with archaic species changed Homo sapiens.
The fate of the Neandertals is the oldest debate in paleoanthropology and one of the longest, most contentious in science. Here I present my perspective on the biological distinction of Neandertals and their role in the emergence of modern people in Europe and the circum-Mediterranean. Neandertals were highly adapted to life in the cold, demanding realm of Europe during the later Pleistocene. This adaptation was strongly biological, and it came at a high energetic price - a price that negatively affected Neandertal reproduction and ultimately resulted in their "extinction." The word "extinction" is in quotes because Neandertals did not go extinct in the classic sense. Rather, both morphological and genetic evidence demonstrate a relatively small, but certainly not insignificant, contribution by them to the earliest modern populations that migrated into their range. From my perspective, the current data best support the assimilation model of modern human origins, first formally presented by two of my graduate students and me almost 25 years ago (Smith et al. 1989), to explain Neandertal-early modern population dynamics. I present an update of that argument here. Also I present my views on why it took modern people so long to establish themselves in Europe and what all this means for the study of biological race in humans.
Outlines theoretical implications of different amounts of gene flow, reviews methods for estimating levels of gene flow in non-human populations, and discusses the evolutionary implications of some current estimates. Discussion centres on gene flow in Drosophila pseudoobscura, checkerspot butterfly Euphydryas editha and salamanders.-P,.J.Jarvis