From Form to Function- Sperm Evolution in Marine Organisms

Abstract

Although sperm share the common function of fertilizing eggs, they exhibit remarkable morphological, molecular and functional diversity across sexually reproducing organisms. This diversity is shaped by evolutionary processes including sexual selection and genetic drift, and contributes to reproductive isolation. In particular, sperm competition, a major mechanism of post-mating sexual selection, drives the evolution of reproductive traits including sperm morphology, sperm heteromorphism, and reproductive fluid composition, while divergence in sperm traits and gamete interactions can contribute to reproductive isolation. However, the functional significance of non-fertilizing sperm morphs in taxa with heteromorph sperm remains poorly understood. In externally fertilizing species, fertilization is often incomplete, yet the roles of sperm competition and reproductive fluids in determining fertilization success remain poorly understood. In this thesis, I investigate how post-mating sexual selection shapes sperm evolution, and how sperm traits play a role in reproductive isolation in eight marine species with contrasting reproductive strategies. In internally fertilizing Littorina snails, imaging, morphometric, and proteomic approaches were used to examine sperm heteromorphism, sperm morphology, and the molecular composition of sperm. In externally fertilizing sea urchins and macroalgae, experimental approaches were used to investigate the effects of sperm competition and reproductive fluids on sperm motility and fertilization success. Parasperm, the non-fertilizing sperm morph in Littorina, exhibited distinct ultrastructural features, including large membrane-bound structures. Parasperm were enriched in proteins associated with energy metabolism, whereas eusperm were enriched in structural proteins. These differences support the hypothesis of functional specialization of the two sperm morphs. Differences in eusperm length between ecotypes of the same Littorina species adapted to different habitats may contribute to reproductive isolation, whereas interspecific variation in eusperm length may reflect differences in sperm competition intensity. Contrary to theoretical expectations and several previous studies, sperm competition in externally fertilizing sea urchins reduced fertilization success, suggesting antagonistic interactions among competing ejaculates. In macroalgae, seminal fluid preferentially enhanced the performance of own versus competitor sperm, whereas female reproductive fluid produced species-specific effects on sperm motility in two hybridizing species, revealing context-dependent roles of reproductive fluids in sperm competition and reproductive isolation. Together, these findings demonstrate that sexual selection shapes sperm evolution through different mechanisms in internal and external fertilizers, acting via sperm morphology, molecular specialization, reproductive fluids and fertilization dynamics. By integrating evidence from both internal and external fertilizers, this thesis advances our understanding of how sexual selection shapes sperm form and function, and how sperm traits play a role in reproductive isolation in marine organisms.