Differential investment in male accessory glands: lessons from a marine fish with alternative reproductive tactics

Male reproductive accessory glands play a number of important roles, including enhancing fertilization success in competitive contexts. Theory predicts that males experiencing greater sperm competition risk (i.e. those adopting the opportunistic tactic) should invest more in accessory glands and ejaculate. However, empirical data show the opposite pattern; males experiencing lower sperm competition risk (i.e. those adopting the conventional guarder tactic) invest more in accessory glands. This pattern has possibly emerged because these organs also function to optimize sperm economy and sometimes also play a role in parental care, which provides more benefits to guarder males. To tease apart these contrasting patterns, we examined tactic-specific investment in and histology of accessory glands, as well as the effect of their fluids on sperm performance in guarder males, using the plainfin midshipman fish (Porichthys notatus). We found that midshipman accessory glands consist of two distinct structures: nodes and lobules, differing in organization and secretory characteristics both between structures and male types. Like other fishes with alternative reproductive tactics, guarder males invested more in accessory glands and in lobules specifically compared to opportunistic sneaker males. Fluids from both lobule and nodes increased sperm velocity in guarder males. Moreover, guarder males increased their investment in accessory glands across the breeding season. Our results suggest that accessory glands may have multiple functions and may even play a role in parental care and olfactory signalling. Our study emphasizes the diversity in form and function of accessory glands and highlights the importance of these organs in reproduction.