Comparative Sperm Proteomics in Mouse Species with Divergent Mating Systems

Abstract

Sexual selection is the pervasive force underlying the dramatic divergence of sperm form and function. Although it has been demonstrated that testis gene expression evolves rapidly, exploration of the proteomic basis of sperm diversity is in its infancy. We have employed a whole-cell proteomics approach to characterize sperm divergence among closely related Mus species that experience different sperm competition regimes and exhibit pronounced variation in sperm energetics, motility and fertilization capacity. Interspecific comparisons revealed significant abundance differences amongst proteins involved in fertilization capacity, including those that govern sperm-zona pellucida interactions, axoneme components and metabolic proteins. Ancestral reconstruction of relative testis size suggests that the reduction of zona pellucida binding proteins and heavy-chain dyneins was associated with a relaxation in sperm competition in the M. musculus lineage. Additionally, the decreased reliance on ATP derived from glycolysis in high sperm competition species was reflected in abundance decreases in glycolytic proteins of the principle piece in M. spretus and M. spicilegus. Comparison of protein abundance and stage-specific testis expression revealed a significant correlation during spermatid development when dynamic morphological changes occur. Proteins underlying sperm diversification were also more likely to be subject to translational repression, suggesting that sperm composition is influenced by the evolution of translation control mechanisms. The identification of functionally coherent classes of proteins relating to sperm competition highlights the utility of evolutionary proteomic analyses and reveals that both intensified and relaxed sperm competition can have a pronounced impact on the molecular composition of the male gamete.

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis in Lepidoptera

“…Despite the more proximate link between proteome composition and molecular phenotypes, transcriptomic analyses far outnumber similar research using proteomic approaches. Nonetheless, recent work confirms the utility of comparative evolutionary proteomic studies in identifying both conserved [ 58 ] and diversifying proteomic characteristics [ 59 ]. We have previously demonstrated a significant correlation in protein abundance between Manduca and Drosophila sperm, although this analysis was limited by the extent of orthology between these taxa [ 9 ].…”

The Old and the New: Discovery Proteomics Identifies Putative Novel Seminal Fluid Proteins in Drosophila

“…Rapid evolution at the molecular level is common for reproductive proteins including SFPs (e.g. (12,(61)(62)(63)). However, extracellular proteins in general exhibit more rapid molecular evolution than proteins restricted to functions within the cell (21)(22)(23).…”

Contrasting patterns of evolutionary constraint and novelty revealed by comparative sperm proteomic analysis

“…Nonetheless, 336 recent work confirms the utility of comparative evolutionary proteomic studies in identifying both 337 conserved [49] and diversifying proteomic characteristics [50]. We have previously demonstrated a 338 significant correlation in protein abundance between Manduca and Drosophila sperm, although this 339 analysis was limited by the extent of orthology between these taxa [9].…”