The case of cortex expansion in hominid evolution
EvoDevo acknowledges that major innovations in evolution involve
extensive alteration processes that go beyond small genetic changes and
gradual accumulation of mutations11EvoDevo researchers
identified five main mechanisms that are involved in the generation of
anatomical diversity through changes in development:
- change in developmental timing (heterochrony)
- change in developmental location/spatial expression (heterotopy)
- changing the sequence of genes being expressed during development
(heterotypy)
- change in the amount of developmental product (heterometry)
- change in the governance of a trait from being environmentally
induced to being genetically fixed (heterocyberny). For example,
evolutionary novelties, such as complex structures or novel organs that
are not present in ancestral groups, may be the result of changes in
developmental timing (i.e., heterochrony). These changes may have been
enabled by either large-scale genetic alterations or by co-option of
existing genetic pathways for new functions. It has been argued that
mutations in regulatory regions that effect the spatial and temporal
expression of whole networks significantly contribute to discontinuous
changes in phenotypic variation and effect the likelihood of trait
retention and its spread in a population (Carroll, 2008). As argued
above, most genes do not code ”for ” a single trait but have
pleiotropic effects prompting them for co-option or gene recruitment.
Similarly, many phenotypic traits have not evolved exerting a single,
distinct feature, but they can be co-opted over evolutionary time to
respond to new challenges. Thus, traits can be exploited in new contexts
or remodeled during ontogenesis. Such processes are termed exaptations,
rather than adaptations (Gould & Vrba, 1982). Exaptations play an
important role in the evolution of cognitive features in humans. In
fact, paleontologists Gould and Vrba claimed that “[m]ost of what
the brain now does to enhance our survival lies in the domain of
exaptation” (Gould & Vrba, 1982; p. 13). Conclusive examples of such
exaptations are the human-specific capacities of reading and arithmetic
that recruit phylogenetically conserved neuronal precursors. Dehaene has
termed the neuroplastic process of exaptation that is characterized by
co-opting existing brain circuits for the acquisitions of novel cultural
operations the “neuronal recycling hypothesis” (Dehane, 2005).
Evolutionary novelties resulting from discontinuous changes of traits
are usually the result of extensive rearrangement processes. The
rearrangement can be driven by gene duplication, regulatory rewiring, or
genetic recombination. Gene duplication produces additional copies of
genes allowing one copy to retain the original function while the other
can undergo evolutionary modification and thereby providing the
potential for novel functions. This is what may drive evolutionary
innovation through the acquisition of new features or adaptations that
enhance the fitness of organisms in their environment. For example,
innovations (i.e., successful novelties) can facilitate new modes of
locomotion, sensory organs, feeding strategies, or reproductive
strategies, allowing individuals of a population to exploit new
ecological niches or more flexibly respond to changing environmental
conditions. In the most successful cases, phenotypic novelties can
trigger adaptive radiation by opening up new ecological opportunities
thereby leading to the rapid diversification and speciation of lineages.
Examples of such key innovations or adaptive break-throughs are the
evolution of flight in birds or insects, the development of flowers in
angiosperms, or the origin of jaws in vertebrates.
An eminent evolutionary innovation in the hominin lineage is the
expansion of the human neocortex. The cortex expansion of humans has
been associated with increased cognitive abilities and behavioral
complexity, which are considered key adaptations in human evolution.
Higher cognitive functions that involve the neocortex include spatial
reasoning, language processing, executive functions, and social
cognition. Complex behavior associated with an expanded human cortex
paved the way for complex problem-solving abilities, abstract reasoning,
the capacity for self-awareness and introspection as well as language,
tool use, symbolic thinking, and the capacity of scaffolded cultural
transmission. These human-specific, complex skills presumably provided
impetus for an increasingly sophisticated, cumulative cultural
evolution.
The expansion of the human cortex is likely the result of a reciprocal
interplay between genetic, developmental, evolutionary, and
environmental factors. A large body of research exists on individual
genes and their combined effects that are involved in the evolutionary
expansion of the human cortex. These candidate genes have been
extensively reviewed elsewhere (Lui et al ., 2011; Sousa et
al ., 2017; Molnar et al ., 2019; Franchini, 2021). Clearly, the
number of species-specific genes cannot account for differences in
functional and behavioral complexity between human and non-human
primates (King & Wilson, 1975). Instead, a relatively small number of
genetic changes that regulate gene expression in both, humans and
chimpanzees, seem to be responsible for the major organismal differences
(Richtsmeier, 2018). In particular, changes that affect the timing or
spatial distribution of gene expression involved in developmental
processes can lead to drastic phenotypic variations and can ultimately
result in phyletic changes (Carroll, 2005; Carroll, et al .,
2001). In this paper, I will use a specific example to explore changes
in developmental timing and argue that heterochronic effects have
probably contributed significantly to the expansion of the human cortex.
A key pathway that plays an important role in cortex expansion includes
the SRGAP2 (Slit-Robo Rho GTPase Activating Protein 2) gene product. TheSRGAP2 gene regulates neuronal migration and differentiation by
inducing filopodia formation, branching of neurons, and neurite
outgrowth, modulates synaptic plasticity, and controls the dynamics
(e.g., the density and morphology) of dendritic spines. One of the
crucial changes that likely underlies the human-specific evolutionary
transition leading to the expansion of the neocortex is the duplication
of the SRGAP2 gene. This duplication occurred in the human
lineage after the divergence from the common ancestor of humans and
chimpanzees. The duplication process gave rise to novel gene variants,SRGAP2B, SRGAP2C, SRGAP2D , which exhibit a high sequence identity
with little genetic variation (Dennis et al. , 2012).
One of the duplicated genes, SRGAP2C , was shown to be
biologically active and expressed at high levels. The resulting protein
does not contain the full-length sequence of the ancestral gene, but is
a truncated version of the original SRGAP2 protein (the latter is named
SRGAP2A in humans). The SRGAP2C protein binds to SRGAP2A protein and
exerts a dominant negative effect resulting in a significant loss of
function of the original SRGAP2 protein. As a result of this functional
loss due to oligomerization, pyramidal neurons that express the
respective genes, migrate faster and take much longer for their
dendritic spines to fully sprout. On the other hand, the delayed growth
of spines of pyramidal neurons allows many more spines to be formed at
full maturation. Thus, the duplicated SRGAP2 genes—in concert
with other genes—triggered a change in the developmental trajectories
and maturation process by influencing the developmental course of
neuronal and synaptic morphogenesis (Dennis et al ., 2012). The
increased migration speed of the cortical neurons on the one hand and
the slower maturation of the synaptic spines on the other hand most
likely contributed to the expansion of the cortex in the lineage ofHomo sapiens (Charrier et al ., 2012; Guerrier et
al ., 2009; Guo & Bao, 2010; Sarto-Jackson et al ., 2017). These
modified cortical maturation processes cannot be observed in
chimpanzees, orangutans, and gorillas (Sudmant et al ., 2010).
Phylogenetic classification analyses confirm that the time frame of
incomplete gene duplication of the SRGAP2 gene correlates with
the phylogenetic transition of the genus Australopithecus to the
genus Homo .
In a nutshell, changes in the timing of brain development over the
course of evolution led to an increase in the neocortical brain surface
(Lui et al . 2011; Rakic 2009) that allowed new cognitive skills
to emerge, which natural selection could act upon. As a result of the
prolonged maturation process, more complex neuronal morphology and
increased neuronal connectivity could develop contributing to the
complexity and the increased multifunctionality of the neocortex in
humans, thus, representing a paradigmatic key innovation in evolution.
Noteworthy, by transmitting the duplicated SRGAP2 gene to the
next generation, what gets passed on is not a particular gene
”for ” cortex expansion that determines a unique human “trait of
an enlarged brain,” but the neuroplastic capacity of a species-typical
developmental trajectory. This capacity is realized by a multitude of
intertwined, neuroplastic processes that effect developmental timing,
most likely in a cascade-like manner.