Sexually Dimorphic Patterns of Cell Proliferation in the Brain Are Linked to Seasonal Life-History Transitions in Red-Sided Garter Snakes

Abstract

Seasonal rhythms in physiology and behavior are widespread across diverse taxonomic groups and may be mediated by seasonal changes in neurogenesis, including cell proliferation, migration, and differentiation. We examined if cell proliferation in the brain is associated with the seasonal life-history transition from spring breeding to migration and summer foraging in a free-ranging population of red-sided garter snakes (Thamnophis sirtalis) in Manitoba, Canada. We used the thymidine analog 5-bromo-2′-deoxyuridine (BrdU) to label newly proliferated cells within the brain of adult snakes collected from the den during the mating season or from a road located along their migratory route. To assess rates of cell migration, we further categorized BrdU-labeled cells according to their location within the ventricular zone or parenchymal region of the nucleus sphericus (homolog of the amygdala), preoptic area/hypothalamus, septal nucleus, and cortex (homolog of the hippocampus). We found that cell proliferation and cell migration varied significantly with sex, the migratory status of snakes, and reproductive behavior in males. In most regions of interest, patterns of cell proliferation were sexually dimorphic, with males having significantly more BrdU-labeled cells than females prior to migration. However, during the initial stages of migration, females exhibited a significant increase in cell proliferation within the nucleus sphericus, hypothalamus, and septal nucleus, but not in any subregion of the cortex. In contrast, migrating males exhibited a significant increase in cell proliferation within the medial cortex but no other brain region. Because it is unlikely that the medial cortex plays a sexually dimorphic role in spatial memory during spring migration, we speculate that cell proliferation within the male medial cortex is associated with regulation of the hypothalamus-pituitary-adrenal axis. Finally, the only brain region where cell migration into the parenchymal region varied significantly with sex or migratory status was the hypothalamus. These results suggest that the migration of newly proliferated cells and/or the continued division of undifferentiated cells are activated earlier or to a greater extent in the hypothalamus. Our data suggest that sexually dimorphic changes in cell proliferation and cell migration in the adult brain may mediate sex differences in the timing of seasonal life-history transitions.

Radial stem astrocytes (aka neural stem cells): Identity, development, physio‐pathology, and therapeutic potential

“…Rodent‐centric views and associated bias are frequently questioned 3 . Adult neurogensis and RSA were characterised in fishes, reptiles, birds, and the majority of wild mammals 120‐125 . Thus adult neurogenesis seems to be evolutionarily conserved, driven by the needs of environmental adaptations.…”

“…3 Adult neurogensis and RSA were characterised in fishes, reptiles, birds, and the majority of wild mammals. [120][121][122][123][124][125] Thus adult neurogenesis seems to be evolutionarily conserved, driven by the needs of environmental adaptations. The details of adult neurogenesis in humans (especially in the hippocampus), however, remain to be elucidated.…”

Reptilian Cognition: A More Complex Picture via Integration of Neurological Mechanisms, Behavioral Constraints, and Evolutionary Context

“…However, on the rare occasion that studies do investigate the mechanisms of reptilian behaviors within an evolutionary framework, they find that the mechanisms governing reptilian behaviors are often quite similar to, and in many cases identical to, mammalian and avian neurological processes, suggesting that their cognitive processes may also be comparable. Much of this work is focused on general, large‐scale differences in the brain, for example, rates of neurogenesis correlated to seasonal life history transitions, sexually dimorphic cognitive traits, or brain size related to success in invasive reptiles . The increase in reptile‐specific cognitive work and the results supporting mechanisms in common with mammals is in many ways similar to the early integrative bird work, which established parity, or nearly so, between the cognitive processes and the mechanisms underlying them in birds and mammals.…”

Sex and Season Affect Cortical Volumes in Free-Living Western Fence Lizards, Sceloporus occidentalis

“…Male cottonmouth snakes (Agkistrodon piscivorus) occupying larger home ranges have larger relative MC volumes than females [Roth et al, 2006]. Red-sided garter snakes (Thamnophis sirtalis) have both seasonal variations within males and sex differences in neurogenesis in several brain regions [Lutterschmidt et al, 2018]. Seasonal differences in neurogenesis in many brain regions, including the MC, were identified in adult Northern Tenerife lizards (Gallotia galloti) [Delgado-Gonzalez et al, 2008] and female tsinling dwarf skinks (Scincella tsinlingensis) [Yang et al, 2017], but it is unclear if these seasonal differences in neurogenesis are associated with differences in cortical volumes or spatial memory.…”