Post-Meiotic Intra-Testicular Sperm Senescence in a Wild Vertebrate

Attila Hettyey,Richard H Wagner,Balázs Vági,Herbert Hoi,Dustin J Penn,Therésa M Jones

doi:10.1371/journal.pone.0050820

Abstract

There is growing interest in sperm senescence, both in its underlying mechanisms and evolutionary consequences, because it can impact the evolution of numerous life history traits. Previous studies have documented various types of sperm senescence, but evidence of post-meiotic intra-testicular sperm senescence in wild animals is lacking. To assess such senescence, we studied within-season changes in sperm motility in the common toad (Bufo bufo), where males produce all sperm prior to the breeding season. We found that males exposed to experimentally induced re-hibernation at the start of the breeding season, that is to experimentally lowered metabolic rates, stored sperm of significantly higher motility than males that were kept under seminatural conditions without females throughout the breeding season. This finding indicates that re-hibernation slows normal rates of sperm ageing and constitutes the first evidence to our knowledge of post-meiotic intra-testicular sperm senescence in a wild vertebrate. We also found that in males kept in seminatural conditions, sperm motility was positively related to the number of matings a male achieved. Thus, our results suggest that post-meiotic intra-testicular sperm senescence does not have a genetically fixed rate and may be modulated by temperature and possibly by mating opportunities.

Highlights

Senescence, which is reduced survival or fertility with increasing age, has been a fundamental problem in evolutionary biology for decades [1,2,3,4] and there is growing interest in sperm senescence [5,6]
We studied sperm quality in isolation from ova because patterns in fertilization success or offspring viability can be confounded by variation in female gamete quality, maternal environmental effects, maternal genetic effects and, most importantly, by variation in the compatibility between male and female gametes [29,30,31]
Our study provides the first evidence to our knowledge of postmeiotic intra-testicular sperm senescence in a wild vertebrate

Summary

Introduction

Senescence, which is reduced survival or fertility with increasing age, has been a fundamental problem in evolutionary biology for decades [1,2,3,4] and there is growing interest in sperm senescence [5,6]. Sperm senescence can reduce sperm quality, which in turn can lower fertilization success and offspring viability, resulting in important consequences for individual fitness [6,7]. Pre-meiotic sperm senescence is the result of damage accumulated in diploid somatic and germ-line cells with advancing male age. The proximate causes include the accumulation of deleterious mutations and a shortening of telomeres in male germ-line cells due to frequent mitosis, the degeneration of nurse cells and other accessory tissue, and a decline in androgen levels or receptor activity [8,9]. Pre-meiotic sperm senescence results in older males having lower quality sperm. Post-meiotic sperm senescence causes individual sperm that had undergone meiosis earlier to be of lower quality

Methods

Results

Conclusion