Brain evolution and development: adaptation, allometry and constraint

Abstract

Phenotypic traits are products of two processes: evolution and development. But how do these processes combine to produce integrated phenotypes? Comparative studies identify consistent patterns of covariation, or allometries, between brain and body size, and between brain components, indicating the presence of significant constraints limiting independent evolution of separate parts. These constraints are poorly understood, but in principle could be either developmental or functional. The developmental constraints hypothesis suggests that individual components (brain and body size, or individual brain components) tend to evolve together because natural selection operates on relatively simple developmental mechanisms that affect the growth of all parts in a concerted manner. The functional constraints hypothesis suggests that correlated change reflects the action of selection on distributed functional systems connecting the different sub-components, predicting more complex patterns of mosaic change at the level of the functional systems and more complex genetic and developmental mechanisms. These hypotheses are not mutually exclusive but make different predictions. We review recent genetic and neurodevelopmental evidence, concluding that functional rather than developmental constraints are the main cause of the observed patterns. How brains evolve: the importance of scaling relationshipsThe components of any adaptive complex by definition undergo coordinated evolution. Brains, bodies and individual brain components therefore exhibit distinctive patterns of correlated evolution. But what do these patterns tell us about the roles of adaptation and constraint in shaping phenotypes? In particular, how and to what extent do constraints imposed by shared developmental programmes dictate allometric relationships between components, limiting their response to selection? These questions have shaped two key debates central to how we view brain evolution: the functional relevance of brain size and the adaptive potential of brain structure [1][2][3]. These debates hinge on whether observed patterns of scaling relationships, between brain and body size or different brain components, are the product of selection to maintain functional correspondence or constraints imposed by shared developmental programmes. Crucially, however, a sound understanding of the significance of scaling relationships in brain evolution has been limited by a lack of data on the genetic and developmental mechanisms that regulate brain size and structure. Here we discuss how recent discoveries about the genetic control of neural development shed new light on the issue.(a) Brain: body coevolution and the importance of size

Genetics of Cerebellar and Neocortical Expansion in Anthropoid Primates: A Comparative Approach

“…These models are potentially non-mutually exclusive and reconcilable at a phenotypic level [Herculano-Houzel et al, 2014], and there has been movement to accommodate some taxon-specific shifts in brain structure within the concerted framework [Clancey et al, 2000[Clancey et al, , 2001Workman et al, 2013]. However, focusing on the "polarised" interpretation of these hypotheses allows us to recognise that these two models implicitly make contrasting predictions about the genetic architecture and proximate basis of variation in brain structure [Airey and Williams, 2001;Montgomery et al, 2016]. The concerted model predicts that variation in the size of different brain regions will be determined by genetic correlations between those structures, i.e., variation in a common set of genes [Montgomery et al, 2016].…”

“…The mosaic model instead predicts that the development of different brain regions must be at least partially distinct in order to facilitate independent evolution. In this case, both co-evolution between brain structures and non-allometric changes in component size may be explained by selection acting of distinct sets of genes [Montgomery et al, 2016].…”

“…However, focusing on the "polarised" interpretation of these hypotheses allows us to recognise that these two models implicitly make contrasting predictions about the genetic architecture and proximate basis of variation in brain structure [Airey and Williams, 2001;Montgomery et al, 2016]. The concerted model predicts that variation in the size of different brain regions will be determined by genetic correlations between those structures, i.e., variation in a common set of genes [Montgomery et al, 2016]. Although cerebellar and cortical cells are produced by distinct progenitor pools [Carletti and Rossi, 2007], concerted expansion could be driven by changes in the global developmental schedules that define the order of neurogenesis across brain structures [Finlay and Darlington, 1995;, extrinsic morphogens that may act on multiple developing brain regions [Menuet et al, 2007;Sylvester et al, 2010], or, in theory, pleiotropic effects of mutations in genes controlling cell division in multiple progenitor pools.…”

“…It remains possible, and indeed likely, that other brain regions show greater evidence of genetic integration. Understanding how and when such genetic and developmental links shape and constrain brain evolution remains central to interpreting the adaptive significance of brain size and structure [Montgomery et al, 2016].…”

“…If the latter is true, do these pleiotropic effects reflect an evolutionary constraint, or have they evolved to maintain the functional relationship between components during brain expansion? These questions will be central to providing a full understanding of brain evolution, and to addressing questions of long-standing interest in evolutionary biology centred on the trade-offs between adaptation and constraint in the genetic basis of composite traits [Montgomery et al, 2016].…”