A drastic shift in the energetic landscape of toothed whale sperm cells

Abstract

Mammalia spermatozoa are a notable example of energetic compartmentalization. While mitochondrial oxidative phosphorylation is restricted to the midpiece, sperm-specific glycolysis operates in the flagellum. Consequently, these highly specialized cells exhibit a clear adaptability to fuel substrates. This plasticity is essential to ensure sperm motility, and is known to vary among species. Here we describe an extreme example of spermatozoa-energetics adaptation. We show that toothed whales exhibit impaired sperm glycolysis, due to gene and exon erosion, and demonstrate that dolphin spermatozoa motility depends uniquely on endogenous fatty acid {beta}-oxidation, but not carbohydrates. Our findings substantiate the observation of large mitochondria in spermatozoa, possibly boosting ATP production from endogenous fatty acids. This unique energetic rewiring emphasizes the physiological body reorganisation imposed by the carbohydrate-depleted marine environment.