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The largely dominant adaptationist argument is currently used as the framework within which hominid brain evolution is explained; however these adaptationist explanations are inherently problematic and only suffice to ‘clutter’ our knowledge of the possible causes of hominid brain evolution. This study addresses the caveats observed in the fossil record and aims to assess the relative influence of structural laws of form, phylogenetic constraints, and adaptive factors during the course of primate and hominid brain evolution. A combination of methods such as variance partitioning, phylogenetic regression procedures and path analysis indicate that constraints have played a critical role in the scaling attributes of the primate and hominid brain. In particular, developmental constraints governing the scaling attributes of the skull and body are shown to explain up to 50 % of the variation in body mass whereas phylogenetic constraints are purported to have played a lesser role (i.e. 0.8 -3.6 %). In addition, the scaling attributes of neural and non-neural components of the cranial vault suggest a highly constrained suite of traits and suggest that as much as 96 % of the variation in both brain mass and residual endocranial space may be explained by correlated scaling with the cranial vault. Constraints are observed to be far more pliable than traditionally thought – a feature highlighted by intraspecific analyses of scaling attributes in humans. Low regression coefficients typical reported for intraspecific curves are shown to arise during development as greater variation in body parameters is allowed with advancing age. Grade shifts in the scaling of brain and body size for primates and other mammalian orders is also emphasised by this current study and it is argued that correlated changes between the brain and body size may not necessarily impact upon the ‘complexity’ of the neural system as the functional integrity may be maintained via higher output states initiated at certain levels of organisation such as at the level of the cortical area. Although constraints should rightfully be given greater coverage in explanations concerning hominid brain expansion, it is only through implementation of research protocols that take a pluralistic approach to an understanding of the role of both constraints and adaptation in the formation of the brain that our interpretation of the likely mechanism for hominid brain expansion may be understood.

Although the human brain has been studied over past decades at morphological and histological levels, much remains unknown about its molecular and genetic mechanisms. Furthermore, when compared with our closest relative the chimpanzee, the human brain strikingly shows great morphological changes that have been often associated with our cognitive specializations and skills. Nevertheless, such drastic changes in the human brain may have arisen not only through morphological changes but also through changes in the expression levels of genes and transcripts. Gene regulatory networks are complex and large-scale sets of protein interactions that play a fundamental role at the core of cellular and tissue functions. Among the most important players of such regulatory networks are transcription factors (TFs) and the transcriptional circuitries in which TFs are the central nodes. Over past decades, several studies have focused on the functional characterization of brain-specific TFs, highlighting their pathways, interactions, and target genes implicated in brain development and often disorders. However, one of the main limitations of such studies is the data collection which is generally based on an individual experiment using a single TF. To understand how TFs might contribute to such human-specific cognitive abilities, it is necessary to integrate the TFs into a system level network to emphasize their potential pathways and circuitry. This thesis proceeds with a novel systems biology approach to infer the evolution of these networks. Using human, chimpanzee, and rhesus macaque, we spanned circa 35 million years of evolution to infer ancestral TF networks and the TF-TF interactions that are conserved or shared in important brain regions. Additionally, we developed a novel method to integrate multiple TF networks derived from human frontal lobe next-generation sequencing data into a high confidence consensus network. In this study, we also integrated a manually curated list of TFs important for brain function and disorders. Interestingly, such “Brain-TFs” are important hubs of the consensus network, emphasizing their biological role in TF circuitry in the human frontal lobe. This thesis describes two major studies in which DNA microarray and RNA-sequencing (RNA-seq) datasets have been mined, directing the TFs and their potential target genes into co-expression networks in human and non-human primate brain genome-wide expression datasets. In a third study we functionally characterized ZEB2, a TF implicated in brain development and linked with Mowat-Wilson syndrome, using human, chimpanzee, and orangutan cell lines. This work introduces not only an accurate analysis of ZEB2 targets, but also an analysis of the evolution of ZEB2 binding sites and the regulatory network controlled by ZEB2 in great apes, spanning circa 16 million years of evolution. In summary, those studies demonstrated the critical role of TFs on the gene regulatory networks of human frontal lobe evolution and functions, emphasizing the potential relationships between TF circuitries and such cognitive skills that make humans unique.

The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)-higher order sensory processing compartments-than the more socially basic Formica subsericea workers. Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina, however, appear to be offset by decreased energetic costs.

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Brain size varies greatly among vertebrates. It has been proposed that the diversity of brain size is produced and maintained through a balance of adaptations to different types and levels of cognitive ability and constraints for adaptive evolution. Phylogenetic comparative studies have made major contributions to our understanding of brain size evolution. However, previous studies have nearly exclusively focused on mammalian and avian taxa and almost no attempts have been made to investigate brain size evolution in ectothermic vertebrates. In my thesis, I studied brain size evolution in two groups of fish with extreme diversity in ecology, morphology and life history, Cichlidae and Syngnathidae. Using phylogenetic comparative methods, I investigated four key questions in vertebrate brain size evolution; cognitive adaptation, sexual selection, phenotypic integration and energetic constraints. I have demonstrated i) that phenotypic integration can link functionally unrelated traits, and this may constrain independent evolution of each part involved or promote concerted evolution of an integrated whole, ii) that brain-body static allometry constrains the direction of brain size evolution, even though the static-allometry showed ability to evolve, allowing evolution of relative brain size under allometric constraints, iii) that the energetic constraints of development and maintenance of brain tissue is an important factor in forming the diversity in brain size in cichlids and syngnathids, both at macroevolutionary and microevolutionary time scales, and iv) that adaptation for feeding and female mating competition may have played key roles in the adaptive evolution of brain size in pipefishes and seahorses. To conclude, my thesis shows the strong benefit of using fish as a model system to study brain size evolution with a phylogenetic comparative framework.

Gyrencephaly (the folding of the surface of the neocortex) is a mammalian-specific trait present in almost all mammalian orders. Despite the widespread appearance of the trait, little is known about the mechanism of its genesis or its adaptive significance. Still, most of the hypotheses proposed concentrated on the pattern of connectivity of mature neurons as main components of gyri formation. Recent work on embryonic neurogenesis in several species of mammals revealed different progenitor and stem cells and their neurogenic potential as having important roles in the process of gyrification. Studies in the field of comparative neurogenesis revealed that gyrencephaly is an evolutionarily labile trait, and that some species underwent a secondary loss of a convoluted brain surface and thus reverted to a more ancient form, a less folded brain surface (lissencephaly). This phenotypic reversion provides an excellent system for understanding the phenomenon of secondary loss. In this review, we will outline the theory behind secondary loss and, as specific examples, present species that have undergone this transition with respect to neocortical folding. We will also discuss different possible pathways for obtaining (or losing) gyri. Finally, we will explore the potential adaptive consequence of gyrencephaly relative to lissencephaly and vice versa.

The human prefrontal cortex (PFC) is associated with complex cognitive behaviors such as planning for the future, memory for serial order, social information processing and language. Understanding how the PFC has changed through time is central to the study of human neural evolution. Here we investigate the expansion of the PFC by measuring relative surface area of the PFC in Pan troglodytes and Homo sapiens. Magnetic resonance images (MRI's) from 8 preserved chimpanzee brains (3 male and 5 female adults) were segmented and measured. The results of this study indicate that there are gross anatomical differences between the chimpanzee and human prefrontal cortex beyond absolute size. The lower surface area to volume ratio in PFC of the chimpanzee when compared to a human indicates less gyral white matter in this region and thus, less associative connectivity. This anatomical evidence of a difference corresponds with the lesser cognitive complexity observed in chimpanzees. / by Ian D. George. / Thesis (M.A.)--Florida Atlantic University, 2009. / Includes bibliography. / Electronic reproduction. Boca Raton, Fla., 2009. Mode of access: World Wide Web.