Reproductive experience drives changes in behaviour and physiology in male California mice, Peromyscus californicus

Paternal experience improves memory and reduces anxiety-like behaviour in males, but it is unclear whether these changes are due to mating, siring offspring or caregiving behaviour. Likewise, paternal males have larger testes, a measure of sperm production, but again, the effects of siring and caregiving experience are difficult to disentangle. We examined behavioural and physiological outcomes in three groups of male mice: (1) virgins, (2) males paired with sterile females (‘nonfathers’) and (3) experienced fathers (experiment 1). Compared to virgins and nonfathers, experienced fathers exhibited increased recognition memory (novel object recognition) and decreased anxiety-like behaviour (elevated plus maze). Virgin males, however, had smaller testes and fewer sperm compared to nonfathers. We then compared the same traits in three additional groups of male mice (nonfathers, nonfathers with experience caring for unrelated pups (‘pup-sensitized nonfathers’) and first-time fathers) to determine whether the behavioural and physiological observations in experiment 1 were due to siring offspring or caregiving, and how rapidly these changes occur (experiment 2). Recognition memory and anxiety-like behaviour did not differ among these three groups, suggesting that caring for a single litter does not recapitulate the behavioural changes observed in experienced fathers (experiment 1). Despite equal mating opportunity, we observed larger testes in first-time fathers compared to nonfathers, suggesting that investment in sperm production may be more plastic than behavioural changes. Finally, we compared pup interactions in pup-sensitized nonfathers and first-time fathers. While pup-sensitized nonfathers were slower to approach pups than first-time fathers, they spent more time grooming pups, whereas first-time fathers invested more time in nest building, suggesting different caregiving behaviours in pup-sensitized males and biological fathers. Taken together, our study reveals that mating, siring and caregiving experience contributes to changes in memory, anxiety-like behaviour and reproductive investment in males of a biparental species. • Pup-sensitized nonfathers approached pups slower than biological fathers. • Pup-sensitized nonfathers groomed pups more than biological fathers. • Biological fathers spent more time nest building than pup-sensitized nonfathers. • More paternal experience improves memory and reduces anxiety-like behaviour. • Virgins had smaller testes and produced fewer sperm than nonfathers but not fathers.