Cortical evolution in mammals: The bane and beauty of phenotypic variability

Abstract

Evolution by natural selection, the unifying theory of all biological sciences, provides a basis for understanding how phenotypic variability is generated at all levels of organization from genes to behavior. However, it is important to distinguish what is the target of selection vs. what is transmitted across generations. Physical traits, behaviors, and the extended phenotype are all selected features of an individual, but genes that covary with different aspects of the targets of selection are inherited. Here we review the variability in cortical organization, morphology, and behavior that have been observed across species and describe similar types of variability within species. We examine sources of variability and the constraints that limit the types of changes that evolution has and can produce. Finally, we underscore the importance of how genes and genetic regulatory networks are deployed and interact within an individual, and their relationship to external, physical forces within the environment that shape the ultimate phenotype.E volution is the change in heritable, phenotypic characteristics within a population that occurs over successive generations. The notion that biological life evolves and that animal forms descend from ancient predecessors has been considered for centuries and, in fact, predates Aristotle (1). However, Charles Darwin was the first to articulate a scientific argument based on extensive observations for a theory of evolution through natural selection. Darwin's theory contains three basic tenets: individuals within a group are variable, variations are heritable, and not all individuals survive (2). Survival is based on selective advantages that particular phenotypic characteristics or behaviors confer to some individuals within a given environmental context. Although in Darwin's time our understanding of the brain was in its infancy and Mendel's Laws of Inheritance were little appreciated, Darwin's assertions regarding evolution through natural selection of adaptive traits, was, and still is, compelling.Recently our understanding of the mechanisms underlying evolution has become more sophisticated, and we appreciate that slight variations in gene sequence can be correlated with alterations of traits and behaviors within and across species. However, an important but often overlooked distinction is the difference between the targets of selection (i.e., phenotypic variations) vs. what natural selection passes on to the next generation (i.e., genes). Although genes are the heritable part of the equation and have a causal, although not always direct, link with some characteristic of the phenotype, genes are not the targets of selection. Genes are indirectly selected for because they covary with the targets of selection, and if the target of selection is adaptive, then genes or portions of the genome replicate and produce a long line of descendants. The direct target of selection is multilayered but can be thought to center around the individual and the unique phenotypic characteristics a...

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