Mass-specific metabolic rate influences sperm performance through energy production in mammals

Abstract

Mass-specific metabolic rate, the rate at which organisms consume energy per gram of body weight, is negatively associated with body size in metazoans. As a consequence, small species have higher cellular metabolic rates and are able to process resources at a faster rate than large species. Since mass-specific metabolic rate has been shown to constrain evolution of sperm traits, and most of the metabolic activity of sperm cells relates to ATP production for sperm motility, we hypothesized that mass-specific metabolic rate could influence sperm energetic metabolism at the cellular level if sperm cells maintain the metabolic rate of organisms that generate them. We compared data on sperm straight-line velocity, mass-specific metabolic rate, and sperm ATP content from 40 mammalian species and found that the mass-specific metabolic rate positively influences sperm swimming velocity by (a) an indirect effect of sperm as the result of an increased sperm length, and (b) a direct effect independent of sperm length. In addition, our analyses show that species with higher mass-specific metabolic rate have higher ATP content per sperm and higher concentration of ATP per μm of sperm length, which are positively associated with sperm velocity. In conclusion, our results suggest that species with high mass-specific metabolic rate have been able to evolve both long and fast sperm. Moreover, independently of its effect on the production of larger sperm, the mass-specific metabolic rate is able to influence sperm velocity by increasing sperm ATP content in mammals.

Sperm bauplan and function and underlying processes of sperm formation and selection

“…The levels of ATP are crucial for sperm swimming performance. This is underscored by the finding that, across species, there is a significant positive relationship between the amount of ATP in sperm and sperm velocity (426,429).…”

“…Explanations for this apparent discrepancy invoked differences in sperm head shape between these species but, since swimming is also influenced by bioenergetics, it is possible that sperm from deer and mouse are obtaining ATP via different pathways which may influence sperm performance together with cell morphology (426). In addition, differences in sperm head shapes between these species may have different impact on drag (186).…”

“…Comparative analyses of actual ATP levels have revealed differences in the amount of sperm ATP in rodents from several lineages (mice, voles, hamsters) and a positive relationship with sperm competition levels (429). Considerable differences were also found in a comparison across mammalian species and, again, a positive association with sperm competition was uncovered (426).…”