Journal of Human Evolution 174 (2023) 103296

Contents lists available at ScienceDirect

Journal of Human Evolution

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

Moving beyond the adaptationist paradigm for human evolution, and

why it matters
Lauren Schroeder a, b, *, Rebecca Rogers Ackermann b, c, *
a
Department of Anthropology, University of Toronto Mississauga, Mississauga, ON, L5L 1C6, Canada
b
Human Evolution Research Institute, University of Cape Town, Rondebosch, 7701, South Africa
c
Department of Archaeology, University of Cape Town, Rondebosch, 7701, South Africa

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

Article history: The Journal of Human Evolution (JHE) was founded 50 years ago when much of the foundation for how
Received 25 April 2022 we think about human evolution was in place or being put in place, providing the main framework for
Accepted 12 November 2022 how we consider our origins today. Here, we will explore historical developments, including early JHE
Available online 15 December 2022
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
Keywords:
links as applied to human evolution. We will focus specifically on how the study of variation itself has
Genetic drift
shifted us away from taxonomic and adaptationist perspectives toward a richer understanding of the
Hybridization
Neutral evolution
processes shaping human evolutionary history, using literature searches and specific test cases to
Natural selection highlight this. We argue that natural selection, gene exchange, genetic drift, and mutation should not be
Phenotypic variation considered individually when considering the production of hominin diversity. In this context, we offer
Evolutionary process 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.
© 2022 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction this classificatory framework, consideration of variation is

predominantly used as a means for determining how different
1.1. Why study variation? two fossils have to be put into different species or subspecies,
information marshaled for the reconstruction of phylogenetic
In the same way that early researchers sought to find key dif- relationships, rather than being a direct focus of study. In addition
ferences that separated groups of living people into ‘races,’ to approaching variation through a decidedly typological frame-
paleoanthropologists have historically (and even today) taken a work, these approaches also frequently (and largely uncon-
similar typological approach when assessing fossil morphology sciously) narrate our origins through a colonial and racialized lens,
(Wolpoff and Caspari, 2000; Marks, 2007; Athreya and Hopkins, a historical legacy of otherizing some and elevating others
2021). By its very nature, the diagnosis of ‘difference’ necessary (Wolpoff and Caspari, 2000; Athreya and Ackermann, 2020;
for making taxonomic assessments, as defined by the Interna- Athreya and Hopkins, 2021).
tional Commission on Zoological Nomenclature (ICZN), compares But understanding phenotypic variation goes well beyond
new specimens to existing hypodigms constructed around a single taxonomic utility, as it provides a link between pattern and process,
holotype individual (ICZN, 1999). Where fossil finds are rare, such allowing us to concentrate on the dynamics of human evolution.
as in paleoanthropology, type specimens are often used to We know that most traits of interest to paleoanthropology have a
represent the average of a species by historical accident rather complex genetic basis (Lewontin, 1974; Lynch and Walsh, 1998;
than because all variation in the species is actually known. Within Houle et al., 2010; Boyle et al., 2017), being continuous, and
therefore generally polygenic, i.e., influenced by more than one
gene. In general, we have a limited grasp of the genetic un-
derpinnings of such morphology (e.g., Mathieson, 2021), with a few
* Corresponding authors.
E-mail addresses: lauren.schroeder@utoronto.ca (L. Schroeder), becky. exceptions (e.g., Aponte, et al., 2021), and while paleogenetic
ackermann@uct.ac.za (R.R. Ackermann). studies can and do provide some insight into evolutionary process,

https://doi.org/10.1016/j.jhevol.2022.103296
0047-2484/© 2022 The Author(s). Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

they often necessarily concentrate on genes of large effect (e.g., classic paper critiquing the ‘adaptationist programme’ and
Lalueza-Fox et al., 2007; Mathieson et al., 2015; Irving-Pease et al., Lande's (1976) incorporation of aspects of the neutral theory into a
2021). Importantly, a focus on morphological variation provides a quantitative genetic framework allowing for the evaluation of fos-
complementary perspective for understanding these processes. sils directly. The discussion of hybridization and its effects was also
However, this focus on phenotypic variation has often resulted in a limited, and was centered primarily within the ‘modern human
tendency toward adaptationist thinking, resulting in the prevalence origins’ context, i.e., whether in an MRE model gene exchange
of what we term the ‘adaptationist paradigm’ in human evolution, existed between the potentially divergent lineages that lead
i.e., a conceptual framework underlying paleoanthropological (collectively) to ‘modern’ people (e.g., Wolpoff et al., 1984).
research that a specific function or adaptation underlies most or Since these early days of JHE, our understanding of the
even all of the variation that we see in the human fossil record. complexities of human evolution, including our understanding of
Here we will briefly reflect on the state of the science when the phenotypic variation, has changed dramatically. We now have a
Journal of Human Evolution (JHE) was first established, in terms of fossil record that is both deeper in time and considerably more
our general understanding of hominin diversity, evolutionary speciose (Fig. 1B), even by conservative estimates. Early hominins
process, and phylogenetic relationships. We will then take a his- are present as early as 6e7 Ma, and there are many points in time
torical perspective, including honing in on early JHE papers that can where species are contemporaneous. Advances in genetics have
be seen as early approaches for considering the link between allowed for the analysis of both living taxa and paleotaxa, providing
variation and evolutionary process, specifically focusing on gene previously unavailable insight into phylogenetic relationships,
exchange and genetic drift, using these as a springboard for hybridization, and an overall deeper understanding of the rela-
exploring where we are today, and where we might go in the tionship between genotype and phenotype (reviews in Gokcumen,
future. We will specifically look at how a variation-based approach 2020; Irving-Pease et al., 2021). In addition, developments in
to understanding evolution has moved us well beyond simplistic evolutionary quantitative genetics have expanded our investiga-
adaptationist narratives of the past by demonstrating how different tory power of evolutionary processes in the fossil record (e.g.,
evolutionary forces work in concert to shape hominin diversity. Hlusko et al., 2016; Melo et al., 2016; Weaver and Gunz, 2018; Brasil
This, in turn, has societal implications for how we interpret et al., 2020; reviews in Weaver, 2018; von Cramon-Taubadel, 2019).
diversity. We conclude by reflecting on a different kind of variation, Within this context, the approach to considering the production of
i.e., demographics of authorship, and how this has the potential to variation has broadened from one that was primarily adaptationist
reshape the science of human evolution going forward. to one that increasingly incorporates genetic drift and gene
exchange as important forces shaping the trajectory of human
1.2. A snapshot of hominin diversity 50 years ago evolution. We will highlight these advances in the next few sections
of this paper, and provide examples of early papers in the journal
In the early 1970s when JHE was established, many researchers that were pioneering in this regard.
still referred to Hominidae, including humans and their extinct
relatives, as separate from Pongidae (the large-bodied apes), as this 2. Quantitative genetics and genetic drift in human
predated the phylogenetic revision based on our molecular evolutionary studies
understanding of the close relationship between humans and
chimpanzees. Indeed, there was limited molecular understanding 2.1. Historical developments
of detailed relationships at all, but this was slowly changing with
advances being made in molecular genetics (e.g., Hoyer et al., 1972). The fundamental mathematical underpinnings of theoretical
At this time, known hominin diversity consisted of only a select population genetics were formulated in the early 20th century
number of taxa from the Homo lineage (Homo habilis, Homo erectus, through the work of S. Wright, R.A. Fisher, and J.B.S. Haldane
Neanderthals, Homo sapiens), and a handful of taxa that were (Provine, 1971). Fisher's (1918) groundbreaking paper formed the
historically lumped into the single genus Australopithecus (i.e., basis for this development, specifically the recognition that
Australopithecus africanus, Australopithecus robustus, and Austral- phenotypic traits are polygenic, and that their inheritance does not
opithecus boisei as shown in Fig. 1A sensu Delson et al., 1977). Well- follow a simple Mendelian model. While this advancement in the
associated archaeology was also fairly limited (Isaac, 1975). The field of genetics provided a more sophisticated, more quantitative
bushy family tree that is so often depicted today was not relevant to approach to evolutionary modeling, the primary process of evolu-
this sparse diversity of hominins, and generally, taxonomic argu- tion (i.e., genetic drift, natural selection, mutation) was a matter of
ments centered on whether the genus Homo was separate from and contention. A good illustration of this is the contrasting viewpoints
contemporaneous with Australopithecus (e.g., Robinson, 1954; of two of population genetics' co-founders. Wright hypothesized
Leakey and Wood, 1973; Robinson and Steudel, 1973), or not (e.g., that genetic drift, acting in small populations, may be an important
Wolpoff, 1971). Owing to this paucity of fossil taxa, the genus Homo force driving evolutionary change (Wright, 1931, 1932, 1970), while
was largely considered to be anagenetic from H. erectus Fisher viewed genetic drift as insignificant, and saw adaptive
onwarddthough much of this discussion was shaped slightly later, evolution through natural selection as the sole and most significant
during the 1980s multiregional evolution (MRE) vs. recent African process (Fisher, 1930). This latter view, termed ‘panselectionism’ by
origin argument related to the emergence of H. sapiens (Thorne and M. Kimura (1983) and discussed in great detail in Gould and Lew-
Wolpoff, 1981; Bra €uer, 1984; Wolpoff et al., 1984; Stringer and ontin's critique of the ‘adaptationist program’ (Gould and Lewontin,
Andrews, 1988). The stark difference between what was known 1979), was much more broadly accepted by biologists, becoming an
about hominin diversity then vs. typical depictions today is illus- almost ubiquitously held position in both genetics and morpho-
trated in Figure 1. logical studies in the mid-20th century.
As we will discuss further below, adaptation via natural selec- One significant deviation from this view came in 1953 when
tion was the primary explanation for the production of hominin G.G. Simpson considered the possible effect that genetic drift may
diversity. There was little attention paid to genetic drift and have had on morphological evolution in the fossil record (Simpson,
nonadaptive processes, given that the journal was established in 1953). Simpson introduced the theoretical model of adaptive zones
1972, only a few years after Kimura (1968) proposed the neutral for driving rapid evolution, hypothesizing that these zones were
theory of evolution, and before both Gould and Lewontin's (1979) dominated by stabilizing selection, but that genetic drift may have
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L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

Figure 1. Comparing a commonly held view of human evolution in 1977 (A) with our contemporary understanding of hominin diversity (B). Temporal ranges of known fossil
hominins are taken from Wood and McRae (2021). Panel A is reprinted from Delson et al. (1977), with permission from Elsevier. Silhouettes in panel B are taken from PhyloPic
(http://phylopic.org).

played an important role when these adaptive zones were crossed lineages (a concept known as the ‘molecular clock’). Second, these
(Simpson, 1953). Loosely mirroring Wright's ‘shifting balance substitutions occur at a much higher rate than would be expected if
theory’ for genotypes (Wright, 1932), this hypothesis represented a most substitutions were adaptive or beneficial, as previously
direct application of population genetics theory to the fossil record. calculated by Haldane (1957). And third, synonymous substitutions
This expansion into macroevolutionary considerations reflected the in noncoding regions of the DNA that do not lead to changes in
growing acceptance and applicability of the synthetic theory or amino acids occur at a much greater rate than nonsynonymous
‘Modern synthesis’ of evolution (Huxley, 1942). However, what was substitutions that do cause amino acid changes (Zuckerkandl and
lacking at the time was a bridge between population genetics with Pauling, 1965b; Salser, 1978). These synonymous substitutions are
its mathematical formulae and allele frequencies that could only be essentially invisible to natural selection, yet they represent the
indirectly and inferentially applied to phenotypes, and actual majority of changes.
evolutionary change at a genotypic level (Kimura, 1983; von An important aspect of the neutral theory that should be
Cramon-Taubadel, 2019). underlined is that it does not disregard the action of natural
This all changed in the mid-1960s with the development of selection entirely. This is a common misconception that has fueled
molecular genetics. Researchers succeeded in determining the many of the criticisms leveled against it as the theory does
amino acid sequences of several proteins found among vertebrate emphasize the action of purifying selection, for removing delete-
taxa, a breakthrough that provided the first opportunity for rious alleles, as playing a large role in neutral explanations (Kimura,
comparing the amount and rate of molecular change among species 1983). Overall, the neutral theory provides a testable mathematical
(Zuckerkandl and Pauling, 1965a). In addition, the detection of framework for application to empirical data, specifically a useful
genetic polymorphisms within species allowed for a more detailed null hypothesis (genetic drift) that if rejected can point to the action
estimation of intrapopulation variability (Lewontin and Hubby, of other evolutionary processes (Kreitman, 1996). While this theory
1966). With these two developments, researchers were finally shifted the dominant adaptationist narrative of evolutionary
able to apply mathematical models of population genetics to change, and hence represented a major contribution to the field of
empirical data, and it was against this backdrop that the neutral population genetics, application to phenotypic evolution had not
theory of evolution was proposed. yet been operationalized.

2.2. The neutral theory 2.3. Quantitative genetics as a means to move beyond the
adaptationist paradigm
The neutral theory of molecular evolution, or the neutral
mutation-random drift hypothesis, claims that most evolutionary The application of the neutral theory to morphological data was
changes are due to random genetic drift (random fixation) of developed through approaches rooted in evolutionary quantitative
selectively neutral or nearly neutral mutants, which are those that genetics, which is the study of the evolution of continuous or
are equivalent in terms of fitness (Kimura, 1968, 1983, 1991). The ‘quantitative’ traits and their underlying genetics (Falconer, 1960;
theory rests mainly on the following premises. First, the rate of Lande, 2000; von Cramon-Taubadel and Schroeder, 2018). Foun-
amino acid or nucleotides substitutions is constant across many dational to this framework is the notion of pleiotropy, the effect of a
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single gene on multiple phenotypic traits, and R. Fisher's 1918 the additive genetic covariances among the traits on the off-
framework of polygenic inheritance, which describes phenotypic diagonal. The relationship between traits at a genetic level that is
traits that are affected by gene variants at multiple loci. These two captured by the G-matrix greatly affects how each trait can respond
concepts emphasize the importance of genetic and phenotypic to the selection gradient (b) in terms of both direction and strength.
variance and covariance as basic measures in quantitative genetic If traits are highly integrated (covary), then they are constrained to
theory (Provine, 1971). follow a similar pattern of directional response to the selection
Another important concept relates to the relationship between pressure, even if selection is acting in multiple directions. In
genotype and phenotype, and its connection to heritability. The contrast, if traits do not covary, they will follow the direction of
basic model of this relationship is that the phenotypic variance of a each separate selection coefficient.
quantitative trait (VP) can be partitioned into genetic variance (VG), Lande and Arnold (1983) provided an extension of this principle
environmental components (VE), and the interaction between as a way of determining the forces of selection acting directly on
these genetic and environmental components (VGE). As a result of traits. This is carried out through the equation: b ¼ P1 s, which
the polygenic inheritance of quantitative traits, the VG component considers selection gradients as partial regression coefficients of
is composed of three sources of genetic variance: additive genetic fitness on traits. In this equation, P1 is the inverse of the pheno-
variance, variance attributed to dominance effects, and variance typic variance/covariance matrix of the traits in question, and s is a
attributed to epistatic interactions (Cheverud, 1988; Lynch and vector of directional selection differentials, i.e., the differences be-
Walsh, 1998). Of these three sources of variance, the additive tween trait means before and after selection. If morphological traits
genetic variance (VA), which refers to variance attributable to the covary significantly, there may be a mismatch in the direction of
additive effects of all inherited gene loci that contribute to a selection and response to that selection, resulting in instances of
particular quantitative trait, is central to the calculation of narrow- indirect selection acting on these selection differentials that
sense heritability (h2), the proportion of VP that can be ascribed to therefore do not confer a fitness benefit.
VA (Falconer and Mackay, 1996; Lynch and Walsh, 1998). This Another major insight from Lande (1979) is that for diverging
measure can be estimated through studies of pedigreed organisms populations under a null hypothesis of genetic drift, the variation of
(e.g., Carson, 2006; Hlusko et al., 2006; Roseman et al., 2010). traits after time t is a function of the G-matrix and the size of these
Narrow-sense heritability is a fundamental variable in the classic populations. The relationship is given by B ¼ G Nte, where B is the
quantitative genetics Breeder's equation (R ¼ h2s), and essentially between-population variance/covariance matrix, t is the time since
provides an estimate of the extent to which a quantitative trait divergence, Ne is the effective population size, and G is the additive
responds to selection, where R is the trait response, and s is the genetic variance/covariance matrix of the source population.
selection differential calculated as the difference between the mean Furthermore, under genetic drift, it is expected that this between-
of the trait before and after selection (Falconer, 1960). This equation group variability (B) is proportional to G. If t and Ne are known,
is central to much of the subsequent contributions to the field, tests of rates of evolution can be performed through the calculation
especially in the application of principles of the neutral theory to

of the generalized genetic distance Nte Dz0 G1 Dz , which follows a
phenotypic evolution.
In 1976, R. Lande developed a theory of evolution, building on c2 distribution under genetic drift, with degrees of freedom equal
the Breeder's equation (Equation 1 in Lande, 1976), that incorpo- to the number of traits. Using a 95% confidence interval, one can
rated aspects of the neutral theory within a quantitative genetic also determine if rates are lower than expected (stabilizing selec-
framework to allow for the evaluation of univariate phenotypic tion), or higher than expected (diversifying selection).
outcomes in fossil populations under models of random genetic These equations and developments have formed the basis for
drift or natural selection, marking a turning point in evolutionary several important advances in the applicability of these techniques
studies. This classic paper also provided the first iteration of a test to phenotypic data, especially after a landmark study by Cheverud
for the null hypothesis of genetic drift based on rates of evolution (1988) provided evidence for the proportionality of G and P
and effective population size, as well as a model for testing matrices (see Roff, 1995 and Sodini et al., 2018 for further support of
Simpson's (1953) proposal of adaptive zones in macroevolution ‘Cheverud's conjecture’), allowing for the substitution of P for G
(Lande, 1976). An additional noteworthy point in this paper that (i.e., phenotype for genotype) in many of the equations given above.
Lande highlights are the difficulties inherent in the estimation of In addition, today we know that for most quantitative morpho-
heritability for fossil populations. He overcomes this by using logical traits of interest, heritability estimates range between 0.3
assumptions based on mammalian models to estimate heritability and 0.5. So like Lande (1976), we make reasonable assumptions of
values in the fossil groups being analyzing (Lande, 1976), something heritabilities based on data from related organisms (e.g., Roseman
that is commonplace today (e.g., Cheverud, 1988; Schroeder et al., et al., 2010), which we can then use to correct our P-matrix.
2014; Baab, 2018; Irish and Grabowski, 2021; Machado et al., 2022). More recently, Ackermann and Cheverud (2002) extended the
Subsequently, many new contributions to the field of quantita- utility of an aspect of Lande's theory, namely the expected
tive genetics were made; however, these early studies were proportionality of G and B across groups (a minimum of two at any
restricted in terms of their application to multivariate quantitative taxonomic level) under genetic drift, by developing a test of this
traits and trait covariance, something that Darwin (1859) also null hypothesis based on linear regression and principal compo-
recognized as important for fully understanding the morphological nent analysis (PCA). First, given the proportionality of G and P (as
response to selective pressures. Another landmark study by Lande per Cheverud, 1988), P is substituted for G. Second, P is decomposed
(1979) provided a solution to this issue with the formulation of into its principal components, and B is calculated by finding the
the multivariate Breeder's equation. The so-called Lande equation variance among principal components projected onto the group
(Dz ¼ Gb) presents the relationship between a vector of trait means. Third, the log-transformed among-group variances (esti-
responses in a population (the difference in those traits before and mated B) are regressed on the log-transformed eigenvalues of P. If
after selection) as a function of the product of the G-matrix (the the slope deviates significantly from one, proportionality is not
additive genetic variance/covariance matrix underlying those traits met, and therefore the null hypothesis of genetic drift can be
in the population) and the vector of selection coefficients (selection rejected.
gradient) acting on those traits (b). The G-matrix is composed of the In addition, advances in genotypeephenotype research in
additive genetic variance of each trait along the diagonal (VA), and pedigreed organisms have elucidated the genetic architecture
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(including heritability and pleiotropic effects) underlying pheno- evolutionary process. Some of these studies have appeared in the
typic diversity, focused mainly on dental variation (e.g., Hlusko pages of JHE. Weaver et al. (2007) showed that the divergence be-
et al., 2004, 2006; Hlusko, 2016; Stojanowski et al., 2018, 2019; tween Neanderthals and recent humans in cranial morphology fol-
Hardin, 2020, but see also Schluter, 1996). These quantitative ge- lowed a neutral pattern. Grabowski and Roseman (2015) used
netic studies have shown that certain phenotypic traits are genet- selection gradients to determine the selection pressures acting on
ically correlated with others (e.g., characters in the dental arcade, hip morphology across a number of hominin taxa. Specifically, they
tooth size, body size), which has major implications for the find evidence for fast rates of evolution and selection on a number of
response of the phenotype to evolutionary pressures, but also for traits in the transition from our last common ancestor with chim-
the application of phylogenetic systematics; an approach that as- panzees (they use extant chimpanzees to model this) to Austral-
sumes independent and uncorrelated characters (Hlusko et al., opithecus afarensis, from A. afarensis to Homo heidelbergensis, and
2006; Grieco et al., 2013). Furthermore, some research has also within later Homo. And finally, Schroeder and Ackermann (2017)
found that this genetic patterning is conserved across multiple used a combination of approaches to assess the relative roles of
mammalian taxa (e.g., Hlusko et al., 2011), which allows for genetic drift and natural selection in the evolution of Homo skull
tentative application to human evolution (Brasil et al., 2020). morphology, finding that genetic drift was widespread across much
As is clear, these developments in the field of evolutionary of this diversification, especially in neurocranial morphology, but
quantitative genetics have provided us with powerful tools for the that natural selection was important for certain aspects of
consideration of phenotypic evolutionary divergence in both morphology related to mastication, particularly for the diversifica-
extant and extinct organisms, beyond the adaptationist paradigm. tion of the Dmanisi hominins from early Homo, and between Homo
Within this framework, one of the most important insights is that rudolfensis and other early Homo groups (Schroeder and Ackermann,
divergence over time between species that happens through ge- 2017). Interestingly, the divergence between Homo naledi and other
netic drift should be proportional to variation seen within species. Homo groups seems to follow a neutral pattern.
This is because divergence by genetic drift is essentially distrib- A few additional studies outside of JHE have applied these
uted randomly across the genome and phenotype, affecting all techniques to the hominin fossil record, focusing on Austral-
traits roughly equally, while adaptive divergence deviates from opithecus, Paranthropus, and the transition to early Homo.
that pattern, with some regions diverging more or less than ex- Schroeder et al. (2014) applied a series of analyses based on
pected because they are being selected for or against. And quantitative genetic theory to assess the evolutionary processes
although there is a complex and sometimes opaque link between underlying skull divergence between potential ancestral groups of
the genotype and phenotype (as has been discussed in detail hominins. They found evidence for selection between Austral-
elsewhere, e.g., Dowell et al., 2010; Milocco and Salazar-Ciudad, opithecus sediba, early Homo, and A. africanus, while transitions
2020; Aponte et al., 2021), as phenotypic variation in morpho- from A. africanus to early Homo followed a neutral pattern
logical characters resembles genetic variation (e.g., Cheverud, (Schroeder et al., 2014). Grabowski (2016) analyzed the evolution of
1988; Hlusko, 2016), these quantitative genetic models and brain and body size in fossil hominins, two traits that have gener-
predictions can be used to answer questions about pattern and ally increased throughout our lineage. They find strong evidence for
process in the human fossil record. selection on brain size during hominin evolution (last common
ancestoreA. afarensis, A. afarensiseH. erectus, H. erectuseH. hei-
2.4. Applications of concepts, past and present delbergensis, H. heidelbergensiseH. sapiens), but not for body size.
This is interpreted as an effect of the covariation between these
Over the past five decades, the analytical and theoretical ad- traits, indicating that body size may not have been under direct
vancements in evolutionary theory detailed earlierdespecially selection pressures during human evolution, but instead may have
those related to the hypothesis testing framework of quantitative increased because of correlated evolution with brain size
genetics, and the inclusion of nonadaptive process as an important (Grabowski, 2016). Similarly, Diniz-Filho and Raia (2017) applied a
mechanism for morphological divergencedhave been widely series of models derived from quantitative genetics to investigate
applied in the broader evolutionary biology literature (e.g., the evolution of brain and body size in Homo floresiensis, and to test
Lofsvold, 1988; Simon et al., 2016; Assis et al., 2017; Rossoni et al., expectations of the Island Rule. Their results indicated a wide-
2017; Machado et al., 2022), but have only recently been explic- spread rejection of neutrality in both the evolution of brain and
itly incorporated in studies of human evolution. body size in H. floresiensis from a putative H. erectus ancestor,
The first direct application of the Lande model to the hominin consistent with directional selection caused by insular dwarfism,
fossil record came in 2004 when Ackermann and Cheverud applied with stronger selection on brain size (Diniz-Filho and Raia, 2017).
regression tests to assess the proportionality of between and within- Several studies by Baab (2018, 2021) have also used aspects of the
group facial variability across a number of hominin taxa, including Lande model to assess cranial variation in the genus Homo, finding
Australopithecus, Paranthropus, and early Homo. They found that evidence for neutral evolution underlying the divergence of a
while genetic drift could be rejected for comparisons involving number of taxa (similar to Schroeder and Ackermann, 2017), but
Australopithecus and Paranthropus, with reconstructed selection also that selection drove the diversification of the frontal bone in
gradients indicating strong selection in the upper-face and zygo- H. erectus. Finally, Hlazo (2018) and Hlazo et al. (2018) identify
matic region, those involving early members of the genus Homo did evidence of natural selection between Australopithecus and Para-
not deviate from expectations of neutrality (Ackermann and nthropus skulls, as well as between eastern and southern African
Cheverud, 2004). Several subsequent studies have successfully Paranthropus, while genetic drift could not be rejected for diver-
applied these techniques within the broader field of biological an- gence between Paranthropus taxa within eastern Africa (Para-
thropology, including analyses of fossil hominins (see below), extant nthropus aethiopicus and Paranthropus boisei). Collectively, these
primates (e.g., Marroig and Cheverud, 2004; Schroeder and von studies underscore the utility of this framework for teasing apart
Cramon-Taubadel, 2017; Schroeder et al., 2022), and recent evolutionary process, but also point to the importance of genetic
humans (e.g., Rolian et al., 2010; Smith, 2011; Savell et al., 2016; drift during human evolution. This is a significant finding, as
Ponce de Leo n et al., 2018; Tran and Schroeder, 2021), demonstrating adaptive explanations have dominated the literature since Darwin,
the robustness of these techniques for our understanding of including within the pages of JHE itself.

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More specific genotypeephenotype quantitative genetic Boyer et al., 1972; Kohne et al., 1972), with morphological studies
approaches to the hominin fossil record have focused on applying only considering genetic drift in a hypothetical sense. For example,
inferences from studies that have used pedigreed data to identify Gabow (1977) considers the evolution of brain size in hominins and
the genetic patterning of certain phenotypic traits. For example, the possible action of genetic drift on small populations with
Hlusko (2016) identified two ratios (molar module component and uneven gene flow. Although Gabow (1977) is distinct from others in
premolaremolar module) describing phenotypic variation in that it incorporates a range of evolutionary processes into a dis-
primate dentition that best reflect the underlying genetic archi- cussion of morphological divergence in human evolution, the
tecture (i.e., are heritable with no pleiotropic effect), and hence can approach lacks proper hypothesis testing.
be used to elucidate evolutionary histories and adaptive shifts Two early papers focusing on evolutionary process, including
through time. They find that these ratios distinguish between genetic drift, that provide an interesting comparison to current
different hominin genera, potentially pointing to different adaptive applications of quantitative genetic theory are Bilsborough (1973,
regimes. A follow-up study by Brasil et al. (2020) showed that the 1976). Using an approach proposed by Lerman (1965) to calculate
molar module component was able to identify genus-level adaptive rates of evolution, Bilsborough estimated rates between various
shifts in hominins, while the premolaremolar module reflected hominin groups, including A. africanus, P. boisei, H. erectus, Ne-
species-level differentiation, indicating that the latter may have anderthals, H. sapiens, and some Middle Pleistocene Homo
been more evolvable through time. In addition, there are several individuals, first only on a subset of cranial vault traits (1973), then
studies that have incorporated specific model-bound approaches on a number of cranial modules and dental traits (1976). The
for testing the congruence of neutral genetic variation (or calculation that was used is based on the Mahalanobis' distance
geographic distance from Sub-Saharan Africa as a proxy for neutral (D) between two groups divided by divergence time
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
genetic differentiation) and phenotypic variability as it applies to ( Dz0 P1 Dz=t). This measure is similar to Lande's estimate of
recent human evolution. Many of these investigations have found evolutionary rate, the generalized genetic distance (GGD) that we
that a substantial number of traits across the skeleton in humans
introduced earlier, i.e., Nte Dz0 G1 Dz (Lande, 1979), which is essen-
have evolved neutrally (Hanihara et al., 2003; Relethford, 2004;
tially a Mahalanobis' distance measure, squared, scaled in this
Roseman, 2004; Hanihara and Ishida, 2005; Harvati and Weaver,
case by effective population size and divergence time. However,
2006; Manica et al., 2007; Hanihara, 2008; von Cramon-Taubadel
unlike Lande's GGD, the application of Lerman's rate of evolution
and Lycett, 2008; Betti et al., 2009, 2010; Smith, 2009; von
does not allow for a detailed hypothesis testing approach to help
Cramon-Taubadel, 2009, 2010; Reyes-Centeno et al., 2017; Betti
elucidate possible evolutionary processes like that offered by a
and Manica, 2018; Rathmann and Reyes-Centeno, 2020). Like that
quantitative genetic framework. This can be seen in Bilsborough's
of the dental studies above, the results of this research have im-
discussion of his results in both papers; he makes inferences
plications for the use of certain traits in analyses, assuming that
about strong selective pressures on cranial capacity and the
those traits are reflective of the underlying genetic architecture.
masticatory region; however, these are based on patterns of dif-
In JHE, some additional phenotypic studies that have used
ferences in the magnitude of rates. Although Bilsborough's papers
quantitative genetic approaches and neutral models of evolution
(1973, 1976) stand out in their innovative approach to assessing
include those that have focused on heritability estimates (e.g.,
morphological variability, the consideration of gene exchange
Hardin, 2020), G-matrix and P-matrix correlation (e.g., de Oliveira
between hominin groups, and what he terms ‘mosaic evolution’ as
et al., 2009), and those that have explicitly incorporated popula-
it relates to differing patterns of cranial and dental morphological
tion structure into their analyses (e.g., Betti et al., 2014); however,
change, the approach is limited in light of the potential of quan-
none of these approaches, except for one twin-study used to esti-
titative genetics.
mate the heritability of having higher average skin temperatures
during exposure to cold (Koertvelyessy and Thompson, 1975), are
reflected in the early days of the journal (1972e1977).1 Rather, what 2.5. Comparing methods: Rates of evolution
we see is a disconnect between studies focused on genetics and
those focused on morphology, mostly due to the lack of a theo- To compare the differences between the two approaches, we
retical and analytical bridge between evolutionary process and the used Lerman (1965) and Lande's GGD to calculate evolutionary
phenotype, as well as the fact that Lande's quantitative genetic rates between a number of hominin groups for 14 cranial vault
phenotype-applicable model was only published in 1976.2 traits based on 8 cranial landmarks (Table 1). Data for this analysis
Regardless of these issues, many early papers did discuss were taken from previous studies (Schroeder, 2015; Schroeder and
morphological evolution and process, usually within an adapta- Ackermann, 2017), and include KNM-ES 11693 (Middle Pleistocene
tionist framework, although some did include discussions of Homo ~200e400 ka; Br€ auer and Leakey, 1986), KNM-ER 406
genetic drift. Of those that did, we do find acknowledgment of the (P. boisei ~1.7 Ma; McDougall and Brown, 2006), MLD 37/38
theoretical developments of Kimura (1968) and King and Jukes (A. africanus ~3.32e2.9 Ma; Latham and Herries, 2004), KNM-ER
(1969), especially their work on mutation rate and the neutral 3883 (H. erectus ~1.5 Ma; Lepre and Kent, 2015), and SAM-AP
theory; however, this was mostly limited to genetic studies (e.g., 4692, a H. sapiens individual from Peer's Cave in South Africa
(~7200 years old; Stynder et al., 2009), and a comparative sample of
86 recent African H. sapiens individuals from the Raymond A. Dart
Collection at the University of the Witwatersrand, and the Iziko
1
Using Scopus, we searched for the terms ‘quantitative genetic/s,’ ‘genetic drift/ Museums of South Africa. We performed comparisons between
random drift/neutral evolution,’ ‘adaptation/adaptive/natural selection,’ and ‘heri-
possible ancestoredescendent pairs, with individual hominin
tability’ in the 347 JHE articles from 1972 to 1977. ‘Genetic drift/random drift/
neutral evolution’ features 18 times, ‘adaptation’ features 77 times, ‘heritability’ specimens used to represent species/group means, and the
features 4 times, and ‘quantitative genetics’ features once. comparative human sample as our model of within-group covari-
2
This is effectively captured in this quote by Jacquard (1977: 734) in JHE, “Finally ance (P-matrix), calculating both the GGD and the rate according to
it is necessary to distinguish two separate fields: one deals with phenotypes, the Lerman (1965). As far as possible, comparisons mirrored those in
purpose is efficiency and the methods are statistics; the other deals with genotypes,
the purpose is understanding and the methods are probabilities. Between these
Bilsborough (1973). Several parameters had to be estimated for the
two fields, we must admit that, in the present state of science, the communications implementation of the GGD, including effective population size,
are at least difficult.” divergence times between species, and generation time. Although
6
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

Table 1
Landmark definitions for traits used in this study.a

Landmark abbreviation Landmark Landmark definition

AP Anterior pterion The most anterior point on the sphenoparietal

suture/the intersection of the parietal, sphenoid and frontal bones
POR Porion The most superior point on the margin of the external auditory meatus
MAS Mastoidale The most inferolateral point on the mastoid process
PN Parietal notch The indentation or angle between the squamous and petrous parts of the
temporal bone, taken on the superior border of the squama temporalis
AST Asterion The junction of the lambdoid, parietomastoid and occipitomastoid sutures
LA Lambda The junction of the sagittal and lambdoid sutures, taken in the midline
BR Bregma The midline junction of the coronal and sagittal sutures
IN Inferior nuchal The most inferior midpoint on the inferior nuchal line
a
The 14 traits extracted from these landmarks are as follows: MASeAST, PNeMAS, ASTePOR, PNePOR, BReLA, INeLA, INeBR, PNeBR, PNeLA, ASTeLA, APeBR, APePN,
APePOR, and APeLA.

these parameters are integral to this approach, and errors in esti- 3. The influence of hybridization on human evolution
mation can have an effect on the eventual interpretation of results,
the GGD is based morphological difference and thus overall pat- 3.1. Historical developments
terns of rates will not be affected. More detail about this analysis
can be found in the Supplementary Online Material (SOM) S1. Hybridization refers to breeding between two distinct taxo-
Analyses were performed in R v. 4.1.0 (R Core Team, 2022). nomic units (species, subspecies, or lineages; see e.g., Taylor and
Results are provided in Table 2. As expected, the findings of the Larson 2019). Experimental and comparative studies examining
GGD analysis provide more detail to the comparisons between the outcomes of hybridization and its implications for the viability
hominin groups in cranial vault traits when compared to Lerman's of taxa, morphological variation, and the expression of the
rate calculation, although the general pattern of rates is similar. phenotype in an evolutionary context have a long history. More
Three comparisons, A. africanus to H. erectus, H. erectus to Middle than 150 years ago, Darwin explored the nature of species and
Pleistocene Homo, and Middle Pleistocene Homo to H. sapiens, varieties in terms of their ability to interbreed, and its effect on size,
show no departure from a neutral model in the GGD analysis, vigor and sterility, including demonstrating that mating between
indicating that genetic drift was likely at play in their divergence. species can be difficult (Darwin, 1859). Although mostly occupied
This result differs from the findings of Bilsborough (1973). For the with the question of sterility and inheritance (Roberts, 1919), he
A. africanus to H. erectus and Middle Pleistocene Homo to recognized the range of variation seen in hybrids, including non-
H. sapiens transitions, Bilsborough (1973) invokes the action of intermediate phenotypes: “There are certain hybrids which,
selection as an explanation for the differentiation between these instead of having, as is usual, an intermediate character between
groups, although rates of evolution may well have been inflated their two parents, always closely resemble one of them” (Darwin,
because of the dates used in the calculations. For the H. erectus to 1859: 256). The basis of Mendel's work on inheritance was also
Middle Pleistocene Homo transition, Bilsborough does suggest grounded in cross-breeding experiments, in this case among vari-
that the differences between the two are much more “econom- eties of one species, providing an understanding of the nature of
ical” (Bilsborough, 1973: 397), and discusses the potential poly- gene segregation and dominance (Mendel, 1866). Although works
typic nature of H. erectus, as well as the possibility of gene such as these were not focused on the deep exploration of hy-
exchange between groups, i.e., “the contribution of each of several bridization and the effects of gene exchange as an evolutionary
possibly ancestral groups to the gene pool of a descendent pop- force per se, they nonetheless illustrate how influential scientists
ulation is directly proportional to the degree of morphological trying to understand evolution and its genetic underpinnings (and
resemblance to that descendent population.” (Bilsborough, 1973: in the absence of genetic data), including adaptation and specia-
398). As for the remaining comparison, A. africanus to P. boisei, a tion, were well aware of the power genetic exchange has to provide
fast rate of evolution was detected in the GGD analysis; an indi- insight into the relationship between the genotype and phenotype.
cation of directional selection (Table 2). This comparison was also In the first half of the 20th century, botanists and zoologists
included in Bilsborough (1973), and selection was proposed as a exploring the effects of hybridization had divergent perspectives,
driver for this transition. drawing disparate conclusions that shaped our understanding of its
Overall, although the pattern of rates is similar across the two importance in different ways (Taylor and Larson, 2019). For
methods, the underlying quantitative genetic theory in the GGD example, botanist G.L. Stebbins considered hybridization to be a
allowed for a more detailed differentiation of various evolutionary creative force for generating genetic diversity (Stebbins, 1950), a
processes using hypothesis testing. And while there are many perspective that was quickly taken up across botany and has long
alternative methods that are available for understanding morpho- been widely accepted (Grant, 1981; Rieseberg, 1997; Arnold, 2015).
logical change through time, such as phylogenetic comparative In contrast, zoologists such as T. Dobzhansky and E. Mayr portrayed
methods (e.g., Go  mez-Robles et al., 2017), the framework of hybridization as rare among animals, and solely a negative selective
evolutionary quantitative genetics provides a series of simple yet agent that reinforced species boundaries (Dobzhansky, 1937; Mayr,
powerful approaches that have advanced our understanding of the 1942), a perspective that persisted for many decades in animal
complex, multiprocess morphological divergence in hominin evo- studies. Although hybridization can lead to decreased fitness in
lution, highlighting the prevalence of genetic drift in human some cases (e.g., Sage et al., 1986), this perspective minimized any
evolution. role of hybridization in generating novelty for selection to act on

7
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

(Barton, 2013). These different foci and perspectives likely had an

The 95% confidence interval for a chi-square distribution at 14 degrees of freedom is (5.63e26.1). GGD values that fall within this interval can be attributed to genetic drift, smaller values indicate stabilizing selection, and
Evolutionary

Genetic drift
Genetic drift
Genetic drift
impact historically on the consideration of the relevance of

Directional
processf

selection
hybridization to human evolution. The racialized implications of
applying hybridization studies to studying people (e.g., in the
context of the prevalent historical narrative of miscegenation; see
Anderson, 2012 and Caspari 2018 for an overview of its application
22.94
24.18
15.42
30.26
GGD

in early physical anthropology) may have also played a role.

size is estimated as 18,500 (Huff et al., 2010), and Homo sapiens is estimated at 13,600 (Henn et al., 2012). Comparisons include average effective population sizes for the two groups being compared.
From the latter part of the 20th century, however, there was a

Effective population size for early hominins (Australopithecus africanus and Paranthropus boisei) is estimated to be 21,000, based on a Pan model (Yu et al., 2004), fossil Homo effective population
growing (albeit not universal) consensus that hybridization has the
100,000 yearse

potential to be a creative force in many contexts, and it is now well-

D units per

(42.28)
Lerman's

(4.08)
(2.31)
(8.66)

established that hybridization has substantially impacted evolution

and speciation of both plants and animals (Anderson, 1953;
2.84
1.32
0.64
1.12

Stebbins, 1959; Rieseberg 1995; Barton, 2001; Mallet, 2007; Abbott

et al., 2013; Arnold, 2015). This includes in mammals, a substantial
The covariance matrix was multiplied by a heritability of 0.4 to take into account imperfect heritability of cranial traits. This estimate was taken from Roseman et al. (2010).

shift in the more than half-century since Stebbins (1959) pointed

2.26
0.62
0.26
0.46
Ne/t

out the dearth of hybridization studies of them. Research now

shows that hybridization is a frequent occurrence in nature,
Estimated effective

including between both closely and distantly related species

population sized

(Mallet, 2005; Mallet et al., 2016), and that the movement of alleles
16050
18500
19750
21000

into lineages can provide novelty that is selectively advantageous,

resulting in hybrid vigor (Grant et al., 2004; Dasmahapatra et al.,
2012; Kirkpatrick and Barrett, 2015; Hanot et al., 2019). Impor-
tantly, this body of research has overturned the historical narrative
of hybridization as solely rare and detrimental (e.g., Mayr, 1942).
corrected by generation

Alleles acquired through hybridization provide new variation (and

length (t in GGD)c
Divergence time

new genetic combinations) that may not have arisen through

29820.00
75480.00
45600.00

mutation alone. Critically, hybridization does not only facilitate

7100

adaptation through the injection of new variation and the subse-

quent action of natural selection, but can introduce genetic variants
that have a selective advantage, facilitating rapid change, though
establishing the adaptive function of introgressed genetic material
Divergence time was calculated as the difference between the estimated mid-point date for each species/group.

remains difficult (Taylor and Larson, 2019). Hybridization can also

introduce neutral variation into lineages, a potential resource for
Divergence time

Abbreviations: D ¼ Mahalanobis Distance; GGD ¼ generalized genetic distance; Ne ¼ Effective population size.
(t in Lerman)b

later evolutionary change. Understanding hybridization is therefore

177500
745500
1887000
1140000

a vital part of understanding the role of both adaptive and neutral

variation, potential drivers of divergence and speciation in human
Generation time is estimated at 25 years for a generalized great ape (Langergraber et al., 2012).

evolution.
Results of Lande's (1979) generalized genetic distance and Lerman's (1965) rates of evolution.

3.2. Model organisms as tools for understanding hybridization in

D2 corrected for

heritabilitya

human evolution
imperfect

10.15
38.97
58.93
65.70

At the time of JHE's establishment, there was very little empir-

ical research being done on hybridization in human evolution; the
research briefly highlighted above occurred within evolutionary
biology, at the time largely outside of the realm of biological
25.37
97.42
147.33
164.26
D2

anthropology. Most of the early JHE papers that considered hy-

Values from Bilsborough (1973) are indicated in parentheses.

bridization were case studies of primate hybrids in captivity and the

wild (e.g., Gijzen, 1973; Bernstein, 1974; Dunbar and Dunbar, 1974).
5.04
9.87
12.14
12.82

However, one JHE paper, in particular, stands out as an exception,

D

namely a theoretical exploration of the effect hybridization might

have had on human ancestors. Roberta Hall (1977) reviews the
Australopithecus africanuseParanthropus boisei

paleobiology and systematics of Canis lupus (wolf) and Canis latrans

(coyote) to develop a model for considering southern African Aus-
larger values indicate directional selection.
Middle Pleistocene HomoeHomo sapiens

Australopithecus africanuseHomo erectus

Homo erectuseMiddle Pleistocene Homo

tralopithecus (i.e., ‘robusts’ and ‘graciles’ as they were considered at

the time). She concludes that wolves/coyotes are ecologically/
behaviorally analogous, including in terms of their breadth of dis-
tribution, and therefore good models for considering variation
across these hominins (see also Hall, 1978). Hall then uses this to
argue that, like wolves and coyotes, A. africanus and Paranthropus
robustus are ‘good’ biological species that nonetheless would have
hybridized to form viable hybrid populations under the right
Comparison

circumstances, retaining distinctiveness at the species but not the

generic level (i.e., they were not different in kind). Although many
Table 2

of the details about Australopithecus and Paranthropus biology are

a

e
b

f
c
d

no longer correct (such as body size and dietary differences),

8
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

nonetheless the mere consideration of them being similarly large size in hybrids, and also skull shape that is somewhat trans-
divergent, but able to hybridize, like wolves and coyotes was gressive relative to their nonhybridized parents (Warren et al.,
exceptional within the field. In considering this topic, rather than 2018). Finally, a recent study of coyote-wolf hybrids also showed
emphasizing species barriers, the author seriously questioned the a high frequency of dental anomalies, dental crowding, and sutural
rigidity of species concepts and especially the biological species anomalies (Zdjelar et al., 2021), providing further support that
concept as it applies to our evolution: “The concept “species” is a these types of traits are indicative of hybridization across a wide
concept and hence a tool of science; it is not a law of nature or a range of mammals.
Procrustean bed into which data must be forced at all costs” (Hall, When lineages/subspecies/species hybridize, the parental
1977: 524). “Following the wolf-coyote model the existence of two groups potentially have different co-adapted gene complexes. In
specific forms does not indicate that no inter-breeding occurred but this context, studies of hybridization in model organisms have
rather that if it did occur it was not sufficient to shatter the provided insight into the genetic architecture of quantitative and
ecological and morphological stability of the two groups” (Hall, behavioral traits, as well as the effect that hybridization can have on
1977: 527). the evolvability of traits (e.g., Gillespie et al., 2020). Mouse crosses
Early approaches such as this laid the foundation for later work have revealed pleiotropic effects on mandibular morphology
including a more widely recognized reticulate model for our origins (Klingenberg et al., 2004), and specific quantitative trait loci related
based on analogs with baboons (Jolly, 2001). Jolly (2001) suggested to long bone length (Norgard et al., 2009). Research on threespine
that Late Pleistocene human population structure was baboon-like, stickleback fish has been particularly valuable for elucidating the
with different species interfertile, albeit morphologically distinct, role of hybridization in contributing standing genetic variation for
and even speculated that humans might have acquired advanta- rapid adaptation (e.g., Schluter and Conte, 2009; Galloway et al.,
geous traits from groups like Neanderthals, suppositions that have 2020; Reid et al., 2021). Similar patterns have been revealed in
turned out to be largely correct (see more below; Jolly, 2016). canids, with a number of positively selected genes associated with
More recent empirical studies examining patterns of skeletal morphology and behavior introduced through hybridization (e.g.,
variation in animal models have extended this approach. These Kays et al., 2010; vonHoldt et al., 2010; Pilot et al., 2021).
studies have provided a way of illuminating population history, Examining patterns of variation when they come together, as
understanding fitness, and potentially determining how selection above, therefore gives us direct insight into underlying genetic ar-
on genes introduced through gene exchange shapes the phenotype, chitecture (however, this can also lead to epistatic effects which are
results of which can be applied to the human past. This research challenging to map, e.g., Mackay, 2014). Developmental anomalies
shows that new variation, even novelty, is produced through associated with, e.g., tooth formation, point to divergence in the
hybridization, and we can see it quite clearly in skeletons of genes responsible for this trait and may affect seemingly unrelated
numerous animals, including coyote-wolf hybrids (Zdjelar et al., traits due to pleiotropy. The novel dental and sutural variation we
2021), baboons (Ackermann et al., 2006, 2014; Eichel and observe in hybrid mammals appears to be minor enough that it
Ackermann, 2016), other primates (Ackermann and Bishop, 2010; does not affect the fitness of individuals (Ackermann et al., 2014).
Buck et al., 2021) and other mammals (Leamy, 1982; Thorpe and Based on the information generated from these model organ-
Leamy, 1983; Ackermann et al., 2010; Warren et al., 2018; Hanot isms, it has been possible to identify evidence for hybridization
et al., 2019). Baboons and canids represent particularly good ana- (which includes possible F1 and later-generation hybrids) in the
logs for hominins in terms of being medium-sized land-based human fossil record.3 This includes evidence for interbreeding
mammals that are geographically widespread, as recognized by between Neanderthals and early humans, in the form of both
Hall and Jolly (and others). atypical dental variation, as well as a wide range of variation more
Studies of pedigreed baboon skulls (Ackermann et al., 2006, generally (Ackermann, 2010; Harvati and Ackermann, 2022). Homo
2014; Eichel and Ackermann, 2016), have examined trait variation sapiens specimens like Oase I and Oase II have been argued to be
in a captive sample of Anubis baboons (Papio anubis), yellow hybrids based on morphology, including their large size and third
baboons (Papio cynocephalus), and their hybrids. First-generation molar megadontia (Ackermann, 2010; Trinkaus et al., 2013;
(F1) hybrids in particular had a high frequency of supernumerary Trinkaus, 2018), and their DNA has confirmed percentages of the
teeth, especially distomolars, and displayed a pattern of expression genome derived from Neanderthals that indicate relatively recent
that differed from ‘normal’ trait variation. F1 hybridsdespecially ancestry (9.90% for Oase I and 6.06% for Oase II; Fu et al., 2015;
malesdalso have enlarged anterior nasal cavities (Eichel and Siska, 2019). Several other late Middle to Late Pleistocene speci-
Ackermann, 2016) and are often large in size more generally, mens, including but not limited to Skhul IV and V, Amud 1, Cro
resulting in increased variation overall. The frequency of atypical Magnon 3, Pavlov 1, Mlade c 5, and individuals from Qafzeh, may
suture morphology is also high in these hybrids. Importantly, these also have morphology consistent with hybridization (Ackermann,
dental and sutural traits persist into later generations, including 2010; Harvati and Ackermann 2022), a hypothesis that requires
second-generation F2 (i.e., F1  F1) animals, backcrosses (B1), and further testing. There is also some evidence that A. afarensis spec-
other recombinant generations (Ackermann et al., 2014), with imens from eastern Africa may have hybridized, presumably with
additional variants like reduced teeth and rotated teeth also other taxa living in relative proximity at the same time, as shown by
present, making this model more relevant to the fossil record the presence of left mandibular fourth molar roots in the corpus of
where we are likely to come across a variety of recombinants and A.L. 198-1 (White and Johanson, 1982; Ackermann, 2010). Austral-
therefore considerable variation. Trait variation such as this is not opithecus afarensis is also known to be highly variable (e.g., Kimbel
unique to baboons; supernumerary teeth are also present in both and Delezene, 2009), which is consistent with our expectations
recent and late Pleistocene ground-squirrel hybrids (Goodwin, from our hybrid mammal models. There is also possible evidence
1998), with a pattern of expression that is rare for nonhybrid
ground squirrels. A confirmed first-generation male beluga/
narwhal hybrid lacks a tusk (actually a tooth), with atypical
3
mandibular teeth unlike what is seen in either parent (Heide- It should also be stated here that while there are other approaches that can be
used to understand the role of past gene flow and migration between groups (e.g.,
Jørgensen and Reeves, 1993; Skovrind et al., 2019), while both Relethford and Blangero, 1990; Weaver, 2018), many of these approaches are reliant
dental and horn anomalies are present in hybrid wildebeest on either genetic data, or large sample sizes for the estimation of within-group
(Ackermann et al., 2010). Like baboons, mice also show relatively covariance, both of which are unfortunately lacking for the fossil record.

9
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

for hybridization in H. floresiensis from the island of Flores, has improved our ability to answer the kinds of questions being
Indonesia, in the form of atypical bilaterally rotated premolars asked by Hall (1977). Finally, it is also worth noting that the
(Ackermann, 2010). divergence time of the grey wolf and coyote is approximately 50 ka
Returning to Hall's (1977) hypothesis, although many of the (vonHoldt et al., 2016), which may make them even better models
details of the paper are no longer correct, given our current for considering recently diverged taxa rather than deeply divergent
understanding of Australopithecus and Paranthropus diversity and ones. Indeed, as argued elsewhere (i.e., Ackermann et al., 2019), the
phylogeny, we can still examine whether this variation, and spe- persistence of ancient allele variants acquired through hybridiza-
cifically the variation within and differences between A. africanus tion (e.g., with Neanderthals, Denisovans) in humans living today,
and P. robustus, is consistent with data from model organisms, especially those related to skin and other factors related to keratin,
especially canids. To date, only one individual specimen from these immunity and high-altitude adaptations (as discussed further
hominin taxa shows evidence for dental or sutural anomalies, below), is in striking parallel to what we see in canids.
P. robustus cranium SK 83 from Swartkrans, which has a supernu- In addition to the identifications above based on empirical evi-
merary lateral incisor in the right maxilla (Ripamonti et al., 1999). dence drawn from model organisms, hybrid individuals have also
Because maxillary incisors are the most common type of super- been proposed in the human fossil record based on other aspects of
numerary tooth (Lavelle and Moore, 1973; Rajab and Hamdan, their morphology, like Lagar Velho 1 (Duarte et al., 1999; Bayle
2002), and unlike distomolars, are not what is seen in the studies et al., 2010), Cioclovina 1 (Soficaru et al., 2006), Vindija (Smith
of model organisms described above, this is not strong evidence for et al., 2015), especially for intermediate or mosaic phenotypes,
hybridization. To further explore the possibility of hybridization although the hybrid status of many of these specimens has been
between these taxa, and the hybrid status of SK 83 in particular, we considered inconclusive (Klein, 2003, 2009) or actively disputed
performed a PCA of maxillary morphology for C. latrans (n ¼ 20), (Tattersall and Schwartz, 1999; Harvati et al., 2007; Stringer, 2012).
C. lupus (n ¼ 20) and their hybrids, C. latrans var. (n ¼ 20; Fig. 2A), Nevertheless, as a whole, we now have substantial morphological
and for P. robustus (n ¼ 7) and A. africanus (n ¼ 4; Fig. 2B). Data were evidence that contemporaneous hominin taxa were interbreeding.
taken from previous studies (Schroeder, 2015; Zdjelar et al., 2021), However, there is still a considerable amount of work to be done on
analyses were performed in PAST v. 4.09 (Hammer et al., 2001), and the phenotype, as will be discussed further below.
details of the analysis can be found in SOM S2 and SOM
Tables S1eS4. Our expectation based on the canid data is that 3.3. Genetic evidence and the hybrid phenotype in human evolution
hybrids will be intermediate to parents (Zdjelar et al., 2021), with
some individuals that are transgressive (outside of the range of the In addition to phenotypic evidence, we also have consid-
parent taxa), a result consistent with previous analyses of both erabledand ever-growingdgenetic evidence for hybridization
baboon species (Ackermann et al., 2016) and mouse subspecies between post-1 Ma lineages in human evolution, the period rele-
(Warren et al., 2018). This is depicted in Figure 2A, where C. lupus vant to the origin of our species, H. sapiens. This genetic evidence
occupies the negative extreme of PC1 and PC2, C. latrans occupies has been well-described elsewhere (e.g., Ackermann et al., 2016;
the positive extreme, with the hybrids falling in between. In our Dannemann and Racimo, 2018; Ackermann et al., 2019; Gokcumen,
hominin analysis, A. africanus and P. robustus are distinct morpho- 2020), and includes evidence for movement of gene variants from
logically, while SK 83 is intermediate and transgressive relative to Neanderthals into early humans (Green et al., 2010; Fu et al., 2014,
both (Fig. 2B). This supports the possibility of hybrid status for SK 2015; Villanea and Schraiber, 2019; Hajdinjak et al., 2021; Prüfer
83, as does its extreme size, the largest in the sample (SOM et al., 2021), and vice versa (Kuhlwilm et al., 2016; Posth et al.,
Table S4), though obviously this hypothesis remains to be tested 2017; Chen et al., 2020), from Denisovans into early humans
further. Clearly, our current evidence drawn from animal models (Reich et al., 2010; Meyer et al., 2012), and from both Neanderthals

Figure 2. Principal component (PC1 vs. PC2) plots of nine maxillary traits in: A) Canis lupus (n ¼ 20; green), Canis latrans (n ¼ 20; yellow), and their hybrids, C. latrans var. (n ¼ 20;
orange); B) Australopithecus africanus (n ¼ 4; grey) and Paranthropus robustus (n ¼ 7; purple) individuals. In panel A, the PCA plot of canids shows an intermediate position for the
hybrids, with the parental taxa being relatively differentiated in shape space. In panel B, the PCA plot of P. robustus and A. africanus shows separation between the two taxa. SK 83
falls outside of both convex hulls. Further detail of each analysis is provided in SOM S2 and Tables S1eS4. All individuals are scaled by their geometric means to reduce the effects of
size variation on the analysis. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article).

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L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

(Prüfer et al., 2014; Slon et al., 2018) and some unknown hominin competitive advantage, a narrative that has not held up under a
(Prüfer et al., 2014) into Denisovans. It also includes evidence for a model that includes the acquisition of advantageous traits from
first-generation child of a Neanderthal mother and a Denisovan local people, and that is also not consistent with our current un-
father (Slon et al., 2018), and for genetic exchanges between ancient derstanding of the cultural sophisticationdin both behavior and
and recent lineages in Africa (Hammer et al., 2011; Lachance et al., material culturedof archaic groups (Sykes, 2020).
2012; Chen et al., 2020; Durvasula and Sankararaman, 2020; Lipson Hybridization among recent hominin taxa has had a lasting
et al., 2020; Wang et al., 2020). Given the growing number of in- impact on human evolution, with its genetic effects remaining a
dividuals and taxa for whom ancient hybridization has been proportionately small but geographically widespread part of
documented, well beyond just hominins (Arnold, 2015; Taylor and human diversity today. Both phenotypic and genetic data are
Larson, 2019), it seems likely that additional studies will continue informative in understanding those dynamics and additionally can
to increase evidence of gene exchange in our past. We do not, provide links between genotype and phenotype (Brand et al.,
however, have comparable genetic evidence for interbreeding 2022). However, we still have very little information linking
among earlier hominins, including all of those outside of our genus, genotype to phenotype, especially in traits of interest to paleoan-
given current limitations around the preservation and methodo- thropologists, such as traits that are taxonomically relevant or
logical capabilities of ancient DNA research. That information is those of known (adaptive) function. This is an easier task for single
only available from phenotypic studies such as those discussed loci of large (known) effect on morphology than for multigene
above (but see Popadin et al., 2022). traits, but the latter characterizes most of our traits of interest in
This paleogenomic research on human origins has allowed us to human evolution. However, two recent studies examine
explore how gene exchange among taxa has shaped phenotypic Neanderthal-derived gene variants in living European people as
variation in humans living today, providing a fuller understanding they relate to cranial/brain form. Gunz et al. (2019) found a link
of the nature of any adaptive benefit or harm as it relates to envi- between Neanderthal gene variants and reduced endocranial
ronmental and cultural factors. Specifically, many of the genes globularity for three regions of the genome, while Gregory et al.
acquired in humans living today through ancient introgression are (2017) found that degree of Neanderthal ancestry was associated
related to skin/hair/keratin characteristics (Sankararaman et al., with Neanderthal-like shape variation in cranial form and brain
2014; Vernot and Akey, 2014; Dannemann and Kelso, 2017), im- structure. Both of these studies highlight the multigene nature of
munity (Abi-Rached et al., 2011; Dannemann et al., 2016), lipid cranial form, and also point to ways in which we can understand
metabolism (Khrameeva et al., 2014), and adaptation to extreme the underlying genetic architecture responsible for morphological
environments (Huerta-S anchez et al., 2014; Hu et al., 2015; Racimo change through time.
et al., 2015; Hackinger et al., 2016). To expand on some of this
research, studies screening for Neanderthal haplotypes in human
genome databases have consistently found evidence for adaptive
introgression from Neanderthals into humans related to skin and 4. The link between pattern and process: future
hair phenotypes, including alleles for hair color and skin pigmen- considerations
tation levels (Vernot and Akey, 2014; Dannemann and Kelso, 2017).
In terms of immunity and adaptation to extreme environments, As we have outlined earlier, over the past 50 years, advances in
there is evidence that both Denisovan and Neanderthal archaic numerous fields such as evolutionary quantitative genetics and
haplotypes associated with altitude adaptation, toll-like receptors ancient DNA, as well as the recognition of the prevalence of genetic
as they relate to innate immunity, and lipid metabolic processes drift and gene exchange in human evolution, have provided our
possibly in relation to diet, have been positively selected in humans discipline with a deeper understanding of the link between
through adaptive introgression (Khrameeva et al., 2014; Racimo morphological variation and evolutionary process outside of an
et al., 2015; Dannemann et al., 2016; Hackinger et al., 2016). Over- adaptationist paradigm. However, there are many avenues of
all, these studies suggest that as humans were leaving Africa, research in these domains that remain to be explored, especially as,
positive selection of alleles introduced through hybridization may despite the increasing evidence for hybridization in human evolu-
have facilitated the range expansion for our species, which is also tion and its importance, there is still fairly limited empirical
consistent with a recent review of the literature that shows that the research on this question outside of the genetics literature. A
most common positive consequence of hybridization is the gain of literature search comparing early and recent years of JHE publica-
adaptive variation (Adavoudi and Pilot, 2022). The persistence of tions indicates that references to hybridization and related terms
acquired traits in living people, including some that are not bene- have not increased meaningfully in 50 years.4 Similarly, although
ficial today (Sankararaman et al., 2014; Simonti et al., 2016; Mozzi there has been a substantial increase in the use of quantitative
et al., 2017), further indicates that they were beneficial or mini- genetic approaches for understanding the relative roles of genetic
mally neutral with respect to fitness in the past, unlike the larger drift and natural selection in hominin evolution, especially with the
proportion of genes that were rapidly eliminated from the gene recent development of statistical toolkits, such as the recently
pool (Juric et al., 2016; Petr et al., 2019). developed R package ‘EvolQG’ v. 0.2-9 by Melo et al. (2016), there
Importantly, under the now-unsupported replacement model of are still several promising avenues for future research and meth-
human origins, where people migrated out of Africa and odological development. Below, we detail several research foci that
outcompeted and/or killed off other groups living in Europe and in our opinion have the potential to enhance our understanding of
Asia, we would likely not observe the full range of genetic and evolutionary process, including the underexplored intersecting
phenotypic diversity that we see on the planet today. In this model nature of these processes, and further illuminate the demographic
with no hybridization, the novel traits we see today that resulted history of hominins.
from genetic exchange would instead have had to evolve through a
long process of random mutation and selection over generations,
4
which may or may not have happened successfully, in the same Using Scopus, we searched for the terms ‘hybridization,’ ‘hybridisation,’ ‘gene
flow,’ ‘introgression,’ ‘hybrid,’ or ‘reticulation/reticulate evolution,’ in the 347 JHE
manner, or in the same timeframe as what occurred due to the articles from 1972 to 1977. Of 347 articles, 25 included at least one of these terms
rapid acquisition of such traits through hybridization. Implicit in (~7%). We did the same thing for the 683 JHE articles from 2016 to 2021, and found
the replacement model was the idea that the migrants had a only a slight relative increase: 56 articles out of 683 (~8%).

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L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

First, we believe that further studies that illuminate the links in the direction of selection and response to that selection, resulting
between the genotype and phenotype (e.g., Gregory et al., 2017; in instances of indirect selection. As selection gradients represent
Gunz et al., 2019) will provide important insight into whether the partial regression coefficients of traits on fitness, these traits
morphological changes that occur as a result of hybridization are therefore do not confer a fitness benefit. This approach can there-
neutral or adaptive. We also need to test morphology, in addition to fore identify traits that are not under selection, and those that are
genes, to understand this relationship, using methodological ap- under indirect selection, i.e., correlated with other traits (such traits
proaches such as those developed in quantitative evolutionary should be avoided in cladistic analyses).
genetics, especially those that can detect signatures of positive To demonstrate the utility of this approach, using the same data
selection in morphology. Importantly, a recent literature review of from our rates of evolution analysis, and focusing on the compar-
hybridization across mammals demonstrated that while negative ison between A. africanus and P. boisei, we reconstruct the direc-
consequences of hybridization appear to be more common than tional selection gradient for this transition following the approach
positive or neutral ones, positive outcomes are typically harder to in Lande and Arnold (1983). A detailed summary of the analysis is
demonstrate than negative ones and therefore may be under- provided in SOM S3 and SOM Table S5. Analyses were performed in
represented in the literature (Adavoudi and Pilot, 2022). In this R v. 4.1.0 (R Core Team, 2022). Results depicted in Figure 3 show
light, we need both to intensify focus on identifying positive that of the 14 cranial vault traits, nine selection coefficients are
outcomes, and also to critically examine narratives of human significantly different from zero (confidence intervals do not
origins that continue to be shaped in ways that minimize the overlap with zero), with four of these showing evidence for indirect
importance of hybridization by pointing out that it is rare and selection, i.e., the trait response is in the opposite direction of the
frequently detrimental. This drumbeat hearkens back to historical selection pressure. Interestingly, parietal bone height (APeBR,
perspectives (e.g., Mayr, 1942) and is inconsistent with the deep PNeBR; see Table 1 for the definition of landmark abbreviations)
and broad literature within organismal biology that highlights seems to be under correlated selection, potentially for superior
hybridization's creative potential. parietal length (BReLA; Table 1).
Second, one important aspect of quantitative genetic theory and Third, there is also a need to investigate whether and how
the Lande model that has been underexplored relates to how hybridization breaks down or relaxes patterns of morphological
genetic architecture, and especially the resultant covariation integration in hominins, and what impact this has on the evolu-
among phenotypic traits, can facilitate or constrain the ability of tionary trajectory of taxa (e.g., Willmore et al., 2009; Nagendran
selection to operate. This is related to the concept of morphological and Schroeder, 2022). Hybridization and introgression often
integration, referring to patterns of coordinated covariance be- result in the recombination of genes in linkage, which results in a
tween traits, and is also intrinsically linked to the concept of decrease in integration between functionally/developmentally
modularity, which describes the apportionment of certain traits related traits, and therefore examining integration in hybrids can
into highly integrated functional/developmental modules that are provide insight into genetic architecture, especially whether inte-
relatively independent of other such modules (Olson and Miller, gration is produced by pleiotropic genes or genes in linkage.
1999). As mentioned earlier, according to the Lande equation if Fourth, there has been little consideration of how hybridization
traits are highly integrated, then they are constrained to follow a affects our phylogenies and interpretation of diversity, which has
similar pattern of directional response to selection; some traits will both practical and conceptual implications, including both the fact
therefore respond even if they are not being directly selected for that phylogenetic trees do not take gene exchange into account and
(Lande, 1979). This is an especially important point to consider theoretical concerns around how we divide species. We also believe
when reconstructing phylogenetic relationships through evolu- that the focus on adaptive (rather than chance) divergence has
tionary time using cladistics, given that cladistic analyses are reliant
on trait independence (Mishler, 1994). We are not the first to point
this out.5 Hlusko (2004) outlined several issues plaguing paleon-
tological research, as well as several incorrect presumptions that
permeate the literature, including trait independence, the adaptive
importance of all traits, and the uniform and slow evolvability of
traits. Although there have been developments on this front using
pedigreed organisms, especially as it pertains to dental variation
(see Hlusko, 2016 for an overview), these approaches rely on
genetic data. One approach from evolutionary quantitative genetics
that can contribute to the solution of these issues when only
considering phenotypic data from fossil hominins is the recon-
struction of selection gradients (Lande and Arnold, 1983;
Ackermann and Cheverud, 2004; Marroig and Cheverud, 2005;
Schroeder and Ackermann, 2017; Schroeder and von Cramon-
Taubadel, 2017). As a reminder, the equation: b ¼ P1 s, describes
the selection gradient as a function of the inverse of the phenotypic
variance/covariance matrix of the traits in question, and the Figure 3. A visual representation of significant selection coefficients necessary to
differences between trait means before and after selection. If produce observed differences in cranial vault morphology between Australopithecus
africanus and Paranthropus boisei. Traits under direct selection (five traits: BReLA,
morphological traits covary significantly, there may be a mismatch
PNePOR, ASTeLA, ASTePOR, and APePOR) are presented by a solid line, whereas
those under indirect selection (four traits: APePN, PNeBR, APeLA, and APeBR) are
presented by a dashed line. Traits that are not under significant selection are not
shown (five traits: MASeAST, PNeMAS, INeLA, INeBR, and PNeLA); however, these
5
Darwin's theory of the ‘correlation of growth’ refers to instances of constraints traits are also likely displaying responses that are due to correlation between traits. 3D
due to trait covariation as a result of growth and development (Darwin, 1859). scan shown is A. africanus specimen MLD 37/38 in the foreground (in gray) super-
Gould and Lewontin expand on this in their critique of the adaptationist program, imposed on Sts 5 (in orange). Landmark abbreviation descriptions are provided in
referring to traits that are by-products of selection elsewhere as a ‘spandrel’ (Gould Table 1. (For interpretation of the references to color in this figure legend, the reader is
and Lewontin, 1979). referred to the Web version of this article).

12
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

served to reify the significance of species differences, and the notion individuals who are pathological in other respects, and further
that some are more fit than others. In this context, the speciose empirical research that more clearly delineates expectations for
picture shown in Figure 1B, with distinct, discrete taxa, is not morphological variation under these different scenar-
consistent with the biological reality discussed here, where species iosdespecially in terms of distinguishing hybridization from
boundaries are fluid and lineages anastomose. As Hall (1977) inbreedingdwill provide considerable insight into population
pointed out, the species concept is a tool of science, and we need dynamics. Scenarios of small population sizes, with associated
to align our taxonomy, narratives and physical depictions of human isolation and expansion/dispersals, suggest that both will be causal
evolution with our current understanding of how species diverge. factors in shaping anatomical variation in the past.
Fifth, Seehausen (2004) theorized a role for hybridization in
adaptive radiations, and recent studies of African cichlids and gue- 5. Final thoughts on the science, society, and scientists
nons have suggested that hybrid swarms can provide the genetic
novelty for adaptive radiations (Parsons et al., 2011; Detwiler, 2019). We wish to emphasize that while there has historically been an
A recent review has also shown widespread genomic evidence for adaptationist perspective to the study of morphological change
hybridization in systems that have undergone adaptive radiations through time in human evolution, it is now clear that the evolu-
(Berner and Salzburger, 2015). Although we do not currently have tionary forces of selection, gene exchange, genetic drift, and
concrete evidence for adaptive radiations in hominins, they certainly mutation have all played a role in our diversification, as highlighted
exist in the evolutionary history of primates (e.g., Marroig and in Figure 4. As has been discussed elsewhere, strict adaptationist
Cheverud, 2005; Aristide et al., 2015; Harrison, 2016; Schroeder thinking does a disservice to understanding the complexity of
et al., 2022), and this is a rich area for further investigation. evolution (Gould and Lewontin, 1979; Koonin, 2016; Kissel and
Sixth, another avenue of research that has been underexplored is Fuentes, 2021), but through methodological, conceptual, and
the application of these approaches to postcranial remains. With re- theoretical advances over the last 50 years, we believe that our
gard to hybridization, most of the work described above on the discipline is ready for a new paradigm. This new paradigm includes
skeletal effects of hybridization has focused on crania. There have a thorough consideration of all four forces, and should also focus on
been several previous studies on mice and primates indicating that how these forces work together to produce variation. For example,
hybrids generally exhibit longer limbs and increased body size rela- because genetic change over evolutionary time frames occurs
tive to their parent taxa (e.g., Carmon, 1963; Leamy, 1982; Thorpe and predominantly through neutral processes (Kimura, 1968, 1991), it is
Leamy, 1983; Leamy, 1992; Kurnianto et al., 1999; Kohn et al., 2001; to be expected that drift would play a major role in shaping the
Warren et al., 2018), but these studies have only rarely looked at shape phenotype, and would be particularly powerful in small, mobile,
variation in detail and have generally not been approached with an relatively isolated communities like we had in the deep past. Like
eye toward interpreting questions relevant to hominin evolution. An selection, genetic drift structures populations into distinct lineages,
exception to this is a recent study by Buck et al. (2021) on hybrid and may have played a large role in diversification throughout
macaques, which investigated variation in the pelvis, and showed that hominin evolution. Hybridization, in turn, occurs between these
the effects of hybridization, in this case, are relatively small, possibly distinct lineages, and while it can play an important role in keeping
because the parent taxa are themselves quite similar morphologically, taxa cohesive and groups evolving together, as discussed here it can
or due to developmental/functional constraints. Future research also lead to evolutionary innovation, including the rapid produc-
needs to explore how hybridization affects shape variation in post- tion of novel and diverse genetic and phenotypic outcomes.
crania with a lens toward interpreting key changes in the hominin Hybridization can result in the transfer/acquisition of neutral
past such as those related to locomotion or childbirth. variation, but can be a particularly powerful force in combination
Similarly, while we do have a few examples of quantitative with selection if new phenotypic outcomes influence fitness, being
genetic studies that have used postcranial data (e.g., Grabowski and either adaptive or maladaptive (Ackermann et al., 2019; Taylor and
Roseman, 2015 on hip morphology, Rolian et al., 2010 on the evo- Larson, 2019). Where selection has acted to differentiate lineages,
lution of human hands and feet, and Savell et al., 2016 on limb hybridization may lead to very different outcomes than it does
lengths in recent humans), the vast majority have focused on skull where genetic drift has done so, given that the latter by definition
morphology. As mentioned earlier, this focus is in part related to the does not involve the evolution of differently coadapted gene com-
disproportionate recovery of cranial, mandibular, and dental fossil plexes, making the understanding of the relative roles of selection
remains compared to postcranial elements, but also due to the and drift key to our understanding of the outcomes of hybridiza-
emphasis on skull morphology for differentiating between taxo- tion, and vice versa. By understanding this interplay among the
nomic groups, which follows from the presumption that post- evolutionary forces, we can gain insight into population dynamics
cranial elements, with their intrinsic functionality, may not be as that further informs our understanding of the past, yet such an
taxonomically informative (McHenry and Brown, 2008). The integrated approach has yet to be well-considered in models of
inclusion of more assessments of postcranial elements within a human evolution.6 Future research into the phenotype that ad-
quantitative genetic framework will allow for a deeper under- dresses this complexity in understanding variation and evolution,
standing of the connection between function and natural selection. and the connection between genotype and phenotype, is essential.
Finally, there have been several recent suggestions that some of We began this article by highlighting how hominin variation has
the skeletal anomalies seen in the human fossil record result from historically been studied within a typological framework, as a means
inbreeding (Trinkaus, 2018; Ríos et al., 2019). Evidence from pri- for classifying rather than an entrance into understanding complex
mates suggests that morphological traits indicative of inbreeding
include reduced size, anencephaly, polydactyly, syndactyly, and
limb malformations (Rawlins and Kessler, 1983; Chalifoux and 6
Using Scopus, we searched for any JHE articles in the 1972e1977 period and the
Elliott, 1986; Nakamichi et al., 1997; Charpentier et al., 2007; van 2016e2021 period that contained mention of a combination of the following terms,
der Valk et al., 2019). In contrast, the evidence to date from grouped into three concept categories: (‘hybridization’ or ‘hybridisation’ or ‘gene
primates and other mammals, discussed earlier, indicates that hy- flow’ or ‘reticulate evolution’ or ‘reticulation’ or ‘introgression’ or ‘hybrid’) and
(‘random drift’ or ‘genetic drift’ or ‘non-adaptive’ or ‘neutral evolution’ or ‘drift’)
bridization results in increased size and extremely rare dental and and (‘natural selection’ or ‘adaptation’). Between 1972 and 1977, there were 2 ar-
sutural traits, in the absence of other associated diseases or ticles out of 347 that made mention of any combination of terms in the three
syndromes. However, traits such as atypical dentition do occur in concept groups, whereas between 2016 and 2021, there were 10 articles out of 683.

13
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

Figure 4. Schematic depicting our current cranial, mandibular, and dental phenotypic evidence for the combined action of genetic drift (yellow ellipses), gene flow (orange ellipses),
and selection (purple ellipses) in the hominin fossil record, based on the quantitative, variation-centered methodological approaches reviewed in this paper. Note that genetic drift
and gene exchange have been shown to be major players in structuring hominin diversity in the last million years, while selection is a major player across lineages ca. 2 Ma. Before
this, we have evidence for drift and possibly gene exchange; however, many of the taxa have yet to be examined using these approaches. Only results of multivariate trait analyses
are shown. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article).

process, and how, in some cases, these approaches have resulted in a our ancestors coming together and exchanging genesdsome of
historical legacy that otherizes some and elevates others (Wolpoff which were neutral but some of which conferred adaptive bene-
and Caspari, 2000; Athreya and Ackermann, 2020; Athreya and fitsdthat facilitated our success as a species by combining traits in
Hopkins, 2021). For the ‘modern human origins’ narrative in new ways. Finally, this history of migration and gene exchange
particular, an adaptationist model where one group was adaptively means that we are not easily parceled into discrete units. These are
superior to another and outcompeted them has resulted in the all important lessons in today's world, providing evidence that can
historical marginalization of Asian taxa and researchers, and ironi- be used to refute the biological basis of meaningful difference, race,
cally (despite the ‘Out of Africa’ focus) in the primitivizing and and othering, in contrast to the historically prevalent narratives of
alienation of African ones (Athreya and Ackermann 2020). A more dominance, superiority, and extinction.
nuanced postadaptationist framework allows us the opportunity to Finally, while considering our mandate for this manuscript, i.e.,
reflect on how we language the past, and the implications of that for to reflect on the history of our topic (especially within JHE) and
people in the present, but it will need to be approached with care and where the field is or should be going in the future, perhaps because
caution. This framework includes a few key messages. First, a lot of we (L.S. and R.R.A.) are women who are either from or currently
the variation we see in the past (and present) is the result of chance, living in South Africa, we became acutely aware that much of the
not meaningful (in terms of fitness) adaptive differences. Second, history relayed above reads as a series of important discoveries by
humans and our ancestors have a deep history of migration, inter- remarkable (largely Western) men. This demographic is also re-
action, and exchange, both within and outside of Africa. Indeed, it is flected in the early papers in JHE, as were very different authorship

14
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

practices, and we asked ourselves whether and to what extent such

demographics have shifted over the lifetime of the journal as the
scientific endeavor has matured. These are important consider-
ations given that the identity and socio-political context of
researchers can shape the narrative direction of the journal and the
science itself (e.g., Athreya and Ackermann, 2020), an issue that is
relevant for JHE going forward.7
Figure 5 provides three infographics, the first looking at data
from the first six years of JHE's outputs, from 1972 to 1977, the
second from the six years immediately following the shift in
editorial oversight to include the USA, from 1986 to 1991, and the
third for the last six years for which we have full data, 2016e2021.
Information on gender and country affiliation is only captured for
first authors; we believe this is a fair reflection of intellectual
ownership, probably more so than weighing all authors equally in
summary statistics. We recognize that characterizing the binary
gender of individuals is problematic, and a crude measure of gender
diversity. We also note that country of affiliation is not a proxy for
‘race,’ but rather pinpoints other characteristics related to power
dynamics, e.g., where the training, funding, and intellectual
ownership resides.
In the earliest years (1972e1977), the majority of papers were
single-authored (63%) and first-authored by men (87%). Only 12%
had 3 or more authors, with the most-authored paper being a
single one with 6 authors. Comparable demographics held from
1986 to 1991, with a majority single authorship (52%) and male first
authorship (82%), though the percentages did decrease in both
cases. In contrast, for the most recent years, only 6% of papers are
single-authored and 80% have 3 or more authors, while male first
authorship has dropped to 59%. This shifting dynamic points to a
discipline whose outputs are produced by larger, collaborative, and
more diverse teams.
However, although there have been substantial demographic
changes in terms of gender parity and author number since JHE was
established, there has been almost no change in terms of country of
origin of the first author. In the initial founding years from 1972 to
1977, 90% of papers were from Western countries, while less than
3% were from Africa and South America, numbers that shifted little
after editorial oversight began to include the USA (1986e1991).
Comparing this to today, there has been virtually no change in first-
authorship from Africa and South America over the last 50 years.
Moreover, in 2016e2021, only 3 of these papers come from South
America, while of the remaining 25 with first author affiliations in
Africa, all but 4 are from South Africa. Turning to Asia, while there
has been an almost 5% increase in first authors from Australasia
from the earliest years to today, from 2016 to 2021, there is only a
single paper where the first author has their primary affiliation in
South Asia, and no first authors have their primary affiliation in
Southeast Asia. Given the journal thrust, a low number of first
authors from South America, where there is not a deep fossil record
of human evolution, might be expected, but similar expectations do
not hold for Africa, South or Southeast Asia, nordgiven this argu-
mentdshould we have very high numbers from other countries
without relevant ancient material, such as North America.
We believe that, in the next 50 years, JHE should focus on using
the journal's power as gatekeepers of a collective norm for the
discipline (sensu Anto  n, 2022) to diversify who holds the status,
power, and authority, and therefore controls the process and
narrative, in order to be a transformative player in the growth of a Figure 5. Demographics of authorship in Journal of Human Evolution: 1972e1977 (A),
richer and more sustainable science. As has recently been pointed 1986e1991 (B), and 2016e2021 (C). Infographics created in Visme (Easy WebContent,
Inc., Rockville).

7 out (Anto n, 2022; Taylor and Zanolli, 2022), JHE has made great
For transparency, one of us (R.R.A.) had a long-term editorial role (Associate
Editor or Book Review Editor) for JHE for more than a decade and a half strides in some respects (e.g., double-blind reviews, gender parity
(2004e2012 and 2014e2020), across the tenures of numerous Editors-in-Chief. in the Editorial Board), but global diversity of authorship is not one
15
L. Schroeder and R.R. Ackermann Journal of Human Evolution 174 (2023) 103296

of those. Anto n details many possible practices that could be R.R.A.) the South African National Research Foundation (L.S., R.R.A.),
incorporated into changing the discipline to one that is more the DST/NRF Centre of Excellence in Palaeosciences (COE-Pal;
diverse and inclusive, and we concur with their suggestions. We R.R.A.), the National Science Foundation (R.R.A.), the Natural Sci-
wish to highlight Anto  n's point that ethically sound, inclusive ences and Engineering Research Council of Canada (Discovery
research needs to be a priority, and based on the data presented Grant RGPIN-2020-04159 to L.S.), and the Connaught Fund of the
here but also our own experiences as scholars from or residing in University of Toronto (New Researcher Award to L.S.). We are
the Global South, helicopter research particularly in Africa (e.g., grateful to the many institutions and individuals for access to
Nature Editorial, 2022) is a key concern. We believe that one comparative fossil and extant mammal, primate, and human
possible reason for such practice is a reliance on academic materials in their care: E. Mbua, P. Kiura, and the National Museums
networks established in formative years as graduate students and of Kenya; the National Museum and House of Culture of Tanzania;
early career scientists, and the difficulty of establishing comparable National Museum of Ethiopia; S. Potze and the Ditsong Museum; B.
relationships across continents and cultures, as well as mandates to Billings and the School of Anatomical Sciences of the University of
train students from your own institution. Given these issues, we the Witwatersrand; B. Zipfel and the Evolutionary Studies Institute
suggest that a key intervention that JHE could make would be to at the University of the Witwatersrand; W. Seconna and the Iziko
actively seek out editorial board membership (including EICs and South African Museum; Y. Haile-Selassie, L.M. Jellema and the
AEs) from diverse backgrounds and geographies, which will begin Cleveland Museum of Natural History; F. Schrenk, O. Kullmer, and C.
the process of breaking down siloed networks, especially as they Hemm and the Senckenberg Forschungsinstitut; Burton Lim and
will provide different perspectives and recommend different po- the Royal Ontario Museum, Robert Feranec and Joseph Bopp and
tential reviewers (we note that the current co-EICs have pledged the New York State Museum, and Darrin Lunde and John Ososky
their commitment to diversity and inclusion in all aspects of the and the Smithsonian National Museum of Natural History. For ac-
journal, and we thus anticipate positive change in the near future8). cess to the canid data, we thank to N. Zdjelar. Finally, we would like
In conjunction, JHE could implement a system for identifying and to thank A.B. Taylor and C. Zanolli for inviting us to contribute this
recruiting reviewers from outside of North America and Europe. piece to ‘The 50th Anniversary of Journal of Human Evolution:
Journal of Human Evolution could also work to incentivize re- Current and Future Directions in Reconstructing our Past’ Virtual
searchers from the Global North to engage meaningfully with Special Issue, as well as L. Hlusko and two anonymous reviewers for
students, researchers, and communities in the countries whose their thoughtful comments on a previous version of our
heritage is being studied, including by encouraging more generous manuscript.
authorship practices (as discussed in Anto  n, 2022), but also by
encouraging practices that include authors from diverse countries
earlier in the stage of research design (such as by explicitly Supplementary Online Material
requesting this information at submission, and therefore normal-
izing it). Supplementary Online Material related to this article can be
Clearly although the journaldand our disciplinedhas made found at https://doi.org/10.1016/j.jhevol.2022.103296.
good strides in terms of the representativity and power of women,
in concert with shifting cultural norms and the maturation of our
discipline and society, there is a considerable way to go to capitalize References
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