Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected

TLDR

In mammals, brain structure mass correlates with nonneuronal cell numbers, yet neuronal scaling varies across structures and between primate and nonprimate clades. The study tests whether these ancestral scaling rules also hold in marsupials, a sister group to eutherians. The authors examined the cellular composition of 10 marsupial species. The data reveal that marsupial brain structure mass scales with nonneuronal cell numbers and that cerebellar neuron counts track cortical neuron counts, mirroring eutherian patterns, but marsupials diverge in that their cerebella are neuron‑rich relative to mass while other brain regions are neuron‑poor, and Australasian species exhibit cortical‑cerebellar neuron ratios akin to artiodactyls and primates, indicating that ancestral Theria neuronal scaling rules have been partially altered and that neuronal size scaling evolves independently of neuronal allocation.

Abstract

In the effort to understand the evolution of mammalian brains, we have found that common relationships between brain structure mass and numbers of nonneuronal (glial and vascular) cells apply across eutherian mammals, but brain structure mass scales differently with numbers of neurons across structures and across primate and nonprimate clades. This suggests that the ancestral scaling rules for mammalian brains are those shared by extant nonprimate eutherians - but do these scaling relationships apply to marsupials, a sister group to eutherians that diverged early in mammalian evolution? Here we examine the cellular composition of the brains of 10 species of marsupials. We show that brain structure mass scales with numbers of nonneuronal cells, and numbers of cerebellar neurons scale with numbers of cerebral cortical neurons, comparable to what we have found in eutherians. These shared scaling relationships are therefore indicative of mechanisms that have been conserved since the first therians. In contrast, while marsupials share with nonprimate eutherians the scaling of cerebral cortex mass with number of neurons, their cerebella have more neurons than nonprimate eutherian cerebella of a similar mass, and their rest of brain has fewer neurons than eutherian structures of a similar mass. Moreover, Australasian marsupials exhibit ratios of neurons in the cerebral cortex and cerebellum over the rest of the brain, comparable to artiodactyls and primates. Our results suggest that Australasian marsupials have diverged from the ancestral Theria neuronal scaling rules, and support the suggestion that the scaling of average neuronal cell size with increasing numbers of neurons varies in evolution independently of the allocation of neurons across structures.