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.