Intra-male reduction in sperm size persists during growth in cuttlefish despite the absence of insemination-site dimorphism.

Abstract

In certain groups of squids and cuttlefish, males display alternative reproductive tactics (ARTs). In squids, size-associated male dimorphism appears in mating posture, spermatophore transfer site (insemination dimorphism), and sperm flagellar length (sperm dimorphism). Sperm dimorphism is closely linked to insemination dimorphism, in which sperm are deposited either at the females external buccal mass or within her mantle cavity. Insemination dimorphism shapes post-copulatory sperm environments, including the mode of storage, the risk of sperm competition, and the site of fertilization. Therefore, sperm dimorphism is regarded as an adaptive consequence of insemination dimorphism. Conversely, in cuttlefish, both large consorts and small female-mimicking (sneaker) males deposit spermatophores in the same region of the female buccal mass, indicating the absence of insemination dimorphism. In Sepia esculenta and Sepia lycidas, sperm located at the distal end of the male reproductive tract possess longer flagella than those near the testis. This pattern is consistent across all male sizes, suggesting that as males grow, they produce sperm with shorter flagella. Additionally, these within-individual differences in sperm size are greater in smaller males and are positively correlated with relative testis mass. These findings indicate that insemination dimorphism is not required for the evolution of dimorphic sperm in cuttlefish. In both squids and cuttlefish, sperm from smaller males must either enter the female receptacle for extended storage or swim faster to compete with the more abundant consort sperm. These unfavorable conditions associated with the sneaker tactic may drive costly sperm evolution.