Understanding primate brain evolution

We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for 'software' programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.     

Modularity in vertebrate brain development and evolution.

Embryonic modularity and functional modularity are two principles of brain organization. Embryonic modules are histogenetic fields that are specified by position-dependent expression of patterning genes. Within each embryonic module, secondary and higher-level pattern formation takes places during development, finally giving rise to brain nuclei and cortical layers. Defined subsets of these structures become connected by fiber tracts to form the information-processing neural circuits, which represent the functional modules of the brain. We review evidence that a group of cell adhesion molecules, the cadherins, provides an adhesive code for both types of modularity, based on a preferentially homotypic binding mechanism. Embryonic modularity is transformed into functional modularity, in part by translating early-generated positional information into an array of adhesive cues, which regulate the binding of functional neural structures distributed across the embryonic modules. Brain modularity may provide a basis for adaptability in evolution.     

Avian brains and a new understanding of vertebrate brain evolution

We believe that names have a powerful influence on the experiments we do and the way in which we think. For this reason, and in the light of new evidence about the function and evolution of the vertebrate brain, an international consortium of neuroscientists has reconsidered the traditional, 100-year-old terminology that is used to describe the avian cerebrum. Our current understanding of the avian brain - in particular the neocortex-like cognitive functions of the avian pallium - requires a new terminology that better reflects these functions and the homologies between avian and mammalian brains.     

Early vertebrate evolution

Debate over the origin and evolution of vertebrates has occupied biologists and palaeontologists alike for centuries. This debate has been refined by molecular phylogenetics, which has resolved the place of vertebrates among their invertebrate chordate relatives, and that of chordates among their deuterostome relatives. The origin of vertebrates is characterized by wide‐ranging genomic, embryologic and phenotypic evolutionary change. Analyses based on living lineages suggest dramatic shifts in the tempo of evolutionary change at the origin of vertebrates and gnathostomes, coincident with whole‐genome duplication events. However, the enriched perspective provided by the fossil record demonstrates that these apparent bursts of anatomical evolution and taxic richness are an artefact of the extinction of phylogenetic intermediates whose fossil remains evidence the gradual assembly of crown gnathostome characters in particular. A more refined understanding of the timing, tempo and mode of early vertebrate evolution rests with: (1) better genome assemblies for living cyclostomes; (2) a better understanding of the anatomical characteristics of key fossil groups, especially the anaspids, thelodonts, galeaspids and pituriaspids; (3) tests of the monophyly of traditional groups; and (4) the application of divergence time methods that integrate not just molecular data from living species, but also morphological data and extinct species. The resulting framework will provide for rigorous tests of rates of character evolution and diversification, and of hypotheses of long‐term trends in ecological evolution that themselves suffer for lack of quantitative functional tests. The fossil record has been silent on the nature of the transition from jawless vertebrates to the jawed vertebrates that have dominated communities since the middle Palaeozoic. Elucidation of this most formative of episodes likely rests with the overhaul of early vertebrate systematics that we propose, but perhaps more fundamentally with fossil grades that await discovery.     

Integrity principle of the evolution of associative centers in the vertebrate brain

Principle trends in the evolution of brain associative centers are discussed. It is demonstrated that in various taxonomic groups the possibilities of adaptive changes, as far as the brain is concerned, go beyond the scope of biological, topographical, and dynamic coordinations, typical for other scopes and systems. The reason for such peculiarity of brain evolution is the multifunctional nature of nerve tissue. This property of nerve tissue allows vertebrates to implement the integrity principle and still preserve the flexibility of the brain, which is highly specialized morphologically and functionally.     

The evolution of vertebrate flight

Flight–defined as the ability to produce useful aerodynamic forces by flapping the wings–is one of the most striking adaptations in vertebrates. Its origin has been surrounded by considerable controversy, due in part to terminological inconsistencies, in part to phylogenetic uncertainty over the sister groups and relationships of birds, bats and pterosaurs, and in part to disagreement over the interpretation of the available fossil evidence and over the relative importance of morphological, mechanical and ecological specializations. Study of the correlation between functional morphology and mechanics in contemporary birds and bats, and in particular of the aerodynamics of flapping wings, clarifies the mechanical changes needed in the course of the evolution of flight. This strongly favours a gliding origin of tetrapod flight, and on mechanical and ecological grounds the alternative cursorial and fluttering hypotheses (neither of which is at present well-defined) may be discounted. The argument is particularly strong in bats, but weaker in birds owing to apparent inconsistencies with the fossil evidence. However, study of the fossils of the Jurassic theropod dinosaur Archaeopteryx , the sister-group of the stem-group proto-birds, supports this view. Its morphology indicates adaptation for flapping flight at the moderately high speeds which would be associated with gliding, but not for the slow speeds which would be required for incipient flight in a running cursor, where the wingbeat is aerodynamically and kinematically considerably more complex. Slow flight in birds and bats is a more derived condition, and vertebrate flapping flight apparently evolved through a gliding stage.     

A cell-molecular approach predicts vertebrate evolution

In contrast to the conventional use of genes to determine the evolution of phenotypes, we have functionally integrated epithelial-mesenchymal interactions that have facilitated lung phylogeny and ontogeny in response to major geologic epochs. As such, this model reveals the underlying principles of lung physiology based on the evolutionary interactions between internal and external selection pressures, providing a novel understanding of lung biology. As a result, it predicts how cell-molecular changes in this process can cause disease and offers counterintuitive insights to diagnosis and treatment based on evolutionary principles.     

Tissue-specific retinal proteins in vertebrate evolution

Studies have been made on water soluble antigens of the retina from man and some animals. In the bovine retina, immunochemical analysis reveals, apart from antigens with a broad and narrow interorganic specificity, organospecific alpha 1- and rho-globulins. Immunochemically, the bovine alpha 1-globulin is partially identical with the same protein of the human retina and completely identical to retinal antigens from cattle; rho-globulin is characterized as an interspecific antigen in man and mammals. Molecules of organospecific alpha 1-globulins from the retina of man and some animals (sheep, camel, horse, cow, pig) do not contain the determinants related to the retinal antigens from fishes, reptiles and birds. In human and mammalian retina, acid neurospecific alpha 1-glycoprotein was found which is topical of the cerebral tissue. Organospecific alpha 1-globulin of the bovine retina is located in the pigment epithelium, in the zone of outer and inner photoreceptor segments; organospecific rho-globulin is distributed in the outer synaptic layer of the retina.     

The neural crest in vertebrate evolution

Vertebrates belong to the group of chordates characterized by a dorsal neural tube and an anteroposterior axis, the notochord. They are the only chordates to possess an embryonic and pluripotent structure associated with their neural primordium, the neural crest (NC). The NC is at the origin of multiple cell types and plays a major role in the construction of the head, which has been an important asset in the evolutionary success of vertebrates. We discuss here the contribution of the rostral domain of the NC to craniofacial skeletogenesis. Moreover, recent data show that cephalic NC cells regulate the activity of secondary brain organizers, hence being critical for preotic brain development, a role that had not been suspected before.     

The compositional evolution of vertebrate genomes

The compositional evolution of vertebrate genomes is characterized: (i) by one predominant conservative mode, in which nucleotide changes occur, but the base composition of DNA sequences in general, and of coding sequences in particular, does not change; and (ii) by three different shifting or transitional modes, in which nucleotide changes are accompanied by changes in the base composition of sequences. Investigations on these evolutionary modes have shed new light on a central problem in molecular evolution, namely the role played by natural selection in modulating the mutational input.This review will present first the intragenomic shifts, the 'major shifts' and the 'minor shift', and then the 'whole-genome', or 'horizontal', shift. In each case, the shifts were preceded and followed by a conservative mode of evolution. This review expands on a previous one [Bernardi, Gene 241 (2000) 3-17], and summarizes the evidence that the changes of the compositional patterns of the genome and their maintenance are controlled by Darwinian natural selection.     

The evolution of early vertebrate photoreceptors

Meeting the challenge of sampling an ancient aquatic landscape by the early vertebrates was crucial to their survival and would establish a retinal bauplan to be used by all subsequent vertebrate descendents. Image-forming eyes were under tremendous selection pressure and the ability to identify suitable prey and detect potential predators was thought to be one of the major drivers of speciation in the Early Cambrian. Based on the fossil record, we know that hagfishes, lampreys, holocephalans, elasmobranchs and lungfishes occupy critical stages in vertebrate evolution, having remained relatively unchanged over hundreds of millions of years. Now using extant representatives of these ‘living fossils’, we are able to piece together the evolution of vertebrate photoreception. While photoreception in hagfishes appears to be based on light detection and controlling circadian rhythms, rather than image formation, the photoreceptors of lampreys fall into five distinct classes and represent a critical stage in the dichotomy of rods and cones. At least four types of retinal cones sample the visual environment in lampreys mediating photopic (and potentially colour) vision, a sampling strategy retained by lungfishes, some modern teleosts, reptiles and birds. Trichromacy is retained in cartilaginous fishes (at least in batoids and holocephalans), where it is predicted that true scotopic (dim light) vision evolved in the common ancestor of all living gnathostomes. The capacity to discriminate colour and balance the tradeoff between resolution and sensitivity in the early vertebrates was an important driver of eye evolution, where many of the ocular features evolved were retained as vertebrates progressed on to land.     

Homeobox genes in vertebrate evolution.

A wide range of anatomical features are shared by all vertebrates, but absent in our closest invertebrate relatives. The origin of vertebrate embryogenesis must have involved the evolution of new regulatory pathways to control the development of new features, but how did this occur? Mutations affecting regulatory genes, including those containing homeobox sequences, may have been important: for example, perhaps gene duplications allowed recruitment of genes to new roles. Here I ask whether comparative data on the genomic organization and expression patterns of homeobox genes support this hypothesis. I propose a model in which duplications of particular homeobox genes, followed by the acquisition of gene-specific secondary expression domains, allowed the evolution of the neural crest, extensive organogenesis and craniofacial morphogenesis. Specific details of the model are amenable to testing by extension of this comparative approach to molecular embryology.     

Appearance of Myelin proteins during vertebrate evolution

Myelin, defined as an arrangement of spirally fused unit membranes, is an acquisition of vertebrates and first appeared during evolution in Gnathostomata. In all species studied PNS and CNS myelins contain the myelin-associated glycoprotein (MAG) and the myelin basic protein (MBP). Throughout phylogeny PNS myelin is characterized by the major P₀ glycoprotein which is called IP in fishes. The PNS myelin proteins did not evolve further except for the addition of P₂ protein from reptiles onward. In Elasmobranchii and Chondrostei, PNS and CNS myelin proteins are similar. CNS myelin of actinopterygian fishes possesses a 36,000 Da protein (36K) in addition to P₀-like IP glycoproteins. In tetrapod CNS myelin, P₀ is replaced by the proteolipid protein (PLP) and the Wolfgram protein (WP). Of particular interest in a transitional phylogenetic sense are the lungfish Protopterus, carrying glycosylated PLP (g-PLP) but no P₀, 36K or WP, and the bichir Polypterus, showing simultaneous presence of P₀, 36K and PLP.

These results indicate that myelin proteins could be valuable molecular markers in establishing vertebrate phylogenetic relationships and in reconstructing the fish-tetrapod transition.     

Molecular evolution of the vertebrate immune system

Adaptive immunity is unique to the vertebrates, and the molecules involved (including immunoglobulins, T cell receptors and the major histocompatibility complex molecules) seem to have diversified very rapidly early in vertebrate history. Reconstruction of gene phylogenies has yielded insights into the evolutionary origin of a number of molecular systems, including the complement system and the major histocompatibility complex (MHC). These analyses have indicated that the C5 component of complement arose by gene duplication prior to the divergence of C3 and C4, which suggests that the alternative complement pathway was the first to evolve. In the case of the MHC, phylogenetic analysis supports the hypothesis that MHC class II molecules evolved before class I molecules. The fact that the MHC-linked proteasome components that specifically produce peptides for presentation by class I MHC appear to have originated before the separation of jawed and jawless vertebrates suggests that the MHC itself may have been present at this time. Immmune system gene families have evolved by gene duplication, interlocus recombination and (in some cases) positive Darwinian selection favoring diversity at the amino acid level.