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

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.

部分物种的雄性个体拥有副性腺（accessory glands）这一额外生殖器官，该类器官为睾丸或输精管的衍生物。这类器官在生殖过程中的功能已得到充分证实，但同时似乎还具备其他尚未被完全阐明的重要功能。本研究针对海生蟾鱼Porichthys notatus的高度复杂的副性腺功能展开探究，该物种存在两种生殖雄性类型：体型较大、负责育幼护卵的‘护卵’雄鱼，以及体型较小、不参与育幼的‘偷袭’雄鱼。尽管两类雄性均拥有副性腺，但护卵雄鱼的副性腺相对于其体型而言显著更大。研究结果显示，副性腺分泌物可强效抑制与不健康鱼卵相关的细菌属生长，而对从健康鱼卵中分离得到的菌株生长无影响。这种抗菌效应在护卵雄鱼的提取物中表现得尤为显著。此外，本研究证实，无论是健康还是不健康的平头蟾鱼（plainfin midshipman）鱼卵，其携带的微生物群落均具有丰富的多样性，但群落组成与丰度存在显著差异。副性腺分泌物对不健康鱼卵来源细菌的高度特异性抑制能力，在一系列符合生态场景的温度与盐度条件下均表现稳定。综合以上生态学与分子生物学观测结果，本研究表明副性腺可通过抗菌物质介导，发挥育幼相关的功能。