Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials

Abstract

Abstract There is considerable debate about whether the partition volumes of the mammalian brain (e.g. cerebrum, cerebellum) evolve according to functional selection, or whether developmental constraints of conserved neurogenetic scheduling cause predictable partition scaling with brain size. Here we provide the first investigation of developmental constraints on partition volume growth, derived from contrast-enhanced micro-computed tomography of hydrogel-stabilized brains from three marsupial species. ANCOVAs of partition vs. brain volume scaling, as well as growth curve comparisons, do not support several hypotheses consistent with developmental constraints: brain partition growth significantly differs between species, or between developing vs. adult marsupials. Partition growth appears independent of adult brain volume, with no discernable growth spurts/lags relatable to internal structural change. Rather, adult proportion differences appear to arise through growth rate/duration heterochrony. Substantial phylogenetic signal in adult brain partitions scaling with brain volume also counters expectations of development-mediated partition scaling conservatism. However, the scaling of olfactory bulb growth is markedly irregular, consistent with suggestions that it is less constrained. The very regular partition growth curves suggest intraspecific developmental rigidity. We speculate that a rigid, possibly neuromer-model-like early molecular program might be responsible both for regular growth curves within species and impressions of a link between neurogenesis and partition evolution.