Reproductive Characteristics of Hermaphrodites in a Trioecious Marine Mussel: Evidence of a Mixed Mating Strategy

Trioecy—the coexistence of males, females, and hermaphrodites within the same population—is one of the rarest sexual systems described in animals. The marine mussel Semimytilus patagonicus is among the few known examples, with hermaphrodites accounting for 95% of individuals. However, the reproductive biology of this dominant phenotype remains poorly understood. In the present study, more than 2500 individuals from natural populations were analyzed to assess sexual maturity, gametogenesis, spawning dynamics, and self-fertilization in hermaphroditic S. patagonicus. The results revealed exceptionally early sexual maturity (L50 = 6.49 mm), with the age at L50 estimated at approximately 68 days based on the fitted model, placing this species among the earliest-maturing bivalves reported to date. Gametogenic development exhibited a seasonal pattern characterized by a high proportion of germinal tissue throughout the study period. Furthermore, variation in male and female gametogenic tissues was synchronized. With respect to gamete release, spawning displayed a protandric pattern, in which the first spawning event was dominated by the release of male gametes (53%), whereas the second was dominated by the release of female gametes (83%), suggesting a mechanism that promotes outcrossing. In addition, fertilization experiments demonstrated that self-fertilization produced normal embryos (~86%) and larval sizes (trochophore: x¯ = 69.4 µm; veliger: x¯ = 118.6 µm) comparable to those obtained through cross-fertilization, indicating a functional capacity for self-fertilization without evidence of inbreeding depression during early developmental stages. This combination of reproductive traits in S. patagonicus is consistent with a mixed mating strategy that balances the advantages of self-fertilization with mechanisms that promote outcrossing. Such a life-history configuration may be particularly adaptive in the dynamic and heterogeneous intertidal environment inhabited by this species. We discuss the implications of these findings for understanding the reproductive dynamics of a trioecious species and their broader significance for the evolution of sexual systems in Animalia.