An agent-based model clarifies the importance of functional and developmental integration in shaping brain evolution

Abstract

AbstractComparisons of vertebrate brain structure suggest a conserved pattern of scaling between components, but also many examples of lineages diverging dramatically from these general trends. Two competing hypotheses of brain evolution seek to explain these patterns of variation by invoking either ‘external’ processes, such as selection driving phenotypic change, or ‘internal’ processes, like developmental coupling among brain regions. Efforts to reconcile these views remain deadlocked, in part due to empirical under-determination and the limitations of ‘relative significance’ debates. We introduce an agent-based model that allows us to simulate brain evolution in a ‘bare-bones’ system and examine the dependencies between variables that may shape brain evolution. Our simulations formalise verbal arguments and interpretations concerning the evolution of brain structure. We illustrate that ‘concerted’ patterns of brain evolution cannot alone be taken as evidence for developmental coupling, or constraint, despite these terms often being treated as synonymous in the literature. Both developmentally coupled and uncoupled brain architectures can represent adaptive mechanisms, depending on the distribution of selection across the brain, life history, and the relative costs of neural tissue. Our model also illustrates how the prevalence of mosaic and concerted patterns of evolution may fluctuate through time in a variable environment, which we argue implies that developmental coupling is unlikely to be a significant evolutionary constraint.