Tactic-specific antimicrobial activity suggests a parental care function for accessory glands in a marine toadfish

Abstract

Males of some species possess extra reproductive organs called accessory glands which are outgrowths of the testes or sperm duct. These organs have a well-established role in reproduction; however, they also appear to have other important functions that are less understood. Here, we investigate the function of the highly complex accessory glands of a marine toadfish, Porichthys notatus , a fish with two reproductive male types: large care-providing ‘guarder’ males and small non-caring ‘sneaker’ males. While both male types have accessory glands, guarder male accessory glands are much larger relative to their body size. We show that accessory gland fluids strongly inhibit the growth of bacterial genera associated with unhealthy eggs and have no effect on the growth of strains isolated from healthy eggs. This antibacterial effect was particularly pronounced for extracts from guarder males. Furthermore, we demonstrate that both healthy and unhealthy plainfin midshipman eggs have diverse but distinct microbial communities that differ in their composition and abundance. The highly specific inhibitory capacity of accessory gland fluid on bacteria from unhealthy eggs was robust across a wide range of ecologically relevant temperatures and salinities. Collectively, these ecological and molecular observations suggest a care function for the accessory gland mediated by antimicrobial agents.

Anatomy of the olfactory system and potential role for chemical communication in the sound‐producing Lusitanian toadfish, Halobatrachus didactylus

“…The role of these accessory glands in reproduction is not yet fully understood; however, their fluids contain muco‐substances and proteins (Modesto & Canário, 2003b) and a diversity of steroids (Modesto et al, 2015) and can prolong sperm motility, possibly enhancing sperm performance during spermiation or fertilization (Modesto, T., unpublished). In the batrachoid Porichtys notatus , these reproductive glands also function in paternal care by inhibiting bacterial growth associated with unhealthy eggs with remarkable specificity (Pepler et al, 2021), and glandular fluids increase sperm velocity in guarder males (Miller et al, 2019). These findings suggest that these glands play important roles in reproduction.…”