The longer the better: longer acrosomes contain more proteins involved in sperm-egg interactions

Abstract

Speciation and sperm competition have been shown to be the major driving forces for sperm morphology variation, swimming velocity and metabolism. We used light microscopy to measure sperm traits and nLC-MS/MS to detect proteomic variation in three species of rodents - promiscuous Apodemus flavicollis, less promiscuous Microtus arvalis, and the least promiscuous Mus musculus musculus. We show that the length of sperm apical hook containing the acrosome is the most variable trait and that this variation is reflected by proteomes on interspecific and intraspecific levels. Thus, we provide potential markers of selection such as Ldhc (in Mus and Apodemus) for long acrosomes which is a gene coding L-lactate dehydrogenase that is involved in sperm motility and Spaca1, which is important in sperm-oocyte fusion), and e.g. Mup17 for short acrosomes - a gene coding a Major urinary protein that likely chelates lipophilic compounds after spermiogenesis. In short, longer acrosomes are characteristic of proteins involved in fertilisation and gluconeogenesis, while shorter acrosomes contain more cytoskeletal proteins important for spermiogenesis. For the first time, we demonstrate that there is an innate and evolvable variability in sperm morphology and corresponding proteomes within species that can be driven by sperm competition to species-specific reproductive optima. Summary statementWe show that interspecific and intraspecific variation in sperm morphology traits are detectable on proteomic level thus providing markers of selection due to sperm competition.