Becoming a Father: Disentangling the Causes and Consequences of Caregiving Behavior in California Mouse Males

Abstract

In mammals, parental care is critical to offspring survival, however, it can also lead to measurable changes in parents. In the biparental California mouse, Peromyscus californicus, fathers actively care for their offspring, including grooming, huddling, retrieving their pups, and building nests. When fathers engage in caregiving behavior, they also experience increased memory, decreased anxiety-like behavior, and structural neuroplasticity of the hippocampus. However, the trigger, reproduction or caregiving experience, and the molecular pathways that regulate these behavioral and neurological changes, remain unclear. In the first chapter, I compared caregiving behaviors in fathers who have cared for their pups and pup-sensitized non-fathers who have cared for unrelated pups, and I found that pup-sensitized non-fathers were slower to approach pups but eventually spent more time grooming pups, whereas fathers spent more time nest-building. I then compared recognition learning, anxiety-like behaviors, and reproductive investment in fathers, pup-sensitized non-fathers, non-fathers with no caregiving experience, and virgins that were socially housed but had no caregiving experience. I found that experienced fathers exhibited increased recognition memory and decreased anxiety-like behavior compared to virgins and non-fathers, and that virgins had smaller testes and fewer sperm compared to non-fathers yet that first-time fathers had larger testes compared to non-fathers. In the second chapter, I first show that hippocampal dendritic spine density is positively associated with males’ caregiving experience. Then, I compared hippocampal gene expression in fathers, non-fathers, and pup-sensitized non-fathers and performed gene ontology, network, and pathway analyses to identify suites of RNA expression patterns associated with caregiving experience. I found that fathers exhibit an upregulation of genes associated with neurogenesis, glutamatergic synapses, neuronal signaling, cellular components of dendritic spines, and some biological pathways previously linked to maternal care, such as regulation of actin cytoskeleton. Together, my results suggest that caregiving behavior induces important behavioral, structural, and transcriptional changes in the brains of males, even if they are caring for offspring that are not their own.