A cost for high levels of sperm competition in rodents: increased sperm DNA fragmentation

Abstract

Sperm competition, a prevalent evolutionary process in which the spermatozoa of two or more males compete for the fertilization of the same ovum, leads to morphological and physiological adaptations, including increases in energetic metabolism that may serve to propel sperm faster but that may have negative effects on DNA integrity. Sperm DNA damage is associated with reduced rates of fertilization, embryo and fetal loss, offspring mortality, and mutations leading to genetic disease. We tested whether high levels of sperm competition affect sperm DNA integrity. We evaluated sperm DNA integrity in 18 species of rodents that differ in their levels of sperm competition using the sperm chromatin structure assay. DNA integrity was assessed upon sperm collection, in response to incubation under capacitating or non-capacitating conditions, and after exposure to physical and chemical stressors. Sperm DNA was very resistant to physical and chemical stressors, whereas incubation in noncapacitating and capacitating conditions resulted in only a small increase in sperm DNA damage. Importantly, levels of sperm competition were positively associated with sperm DNA fragmentation across rodent species. This is the first evidence showing that high levels of sperm competition lead to an important cost in the form of increased sperm DNA damage.

The hidden ageing costs of sperm competition

“…Species‐specific differences in the level of sperm competition could also shape diverse patterns of reproductive ageing in males (and thus various patterns of sex differences in reproductive ageing). Interestingly, a comparative analysis performed across 18 species of rodents maintained in laboratory conditions revealed a positive relationship between levels of sperm competition and DNA fragmentation among sperm (delBarco‐Trillo et al ., 2016), which suggests that interspecific differences in the level of sperm competition can explain between‐species differences in sperm integrity. Whether these differences are exacerbated with increasing age and occur in the wild is unknown but this clearly deserves attention.…”

Chemosensory and hyperoxia circuits in C. elegans males influence sperm navigational capacity

“…Environmental exposures during early development could be indicative of future stressful conditions. For example, O 2 and mitochondria are important for fertility, but they also produce toxic ROS, which is associated with DNA damage and reduced fertilization success in many species [ 20 , 75 ]. In environments where ROS levels are likely to be elevated, C .…”

“…Oxidative stress is thought to be a major factor in male infertility and sperm DNA damage [ 16 – 18 ]. In rodent species with different sperm competition levels, increased competition is associated with increased sperm oxidative metabolism, motility performance, and DNA damage measured in vitro [ 19 , 20 ]. The extent to which sperm rely on aerobic metabolism may vary among environmental conditions.…”

Feed-backs among inbreeding, inbreeding depression in sperm traits, and sperm competition can drive evolution of costly polyandry

“…; delBraco‐Trillo et al. ), and that increased investment in sperm following increased sperm competition is likely to trade‐off against other male traits (Snook ), including other sperm traits (Moore et al. ; Helfenstein et al.…”

“…where β determines the cost of a single sperm cell (Engqvist 2012;Bocedi and Reid 2016). There is ample empirical evidence that sperm is costly Pitnick et al 2009;delBraco-Trillo et al 2016), and that increased investment in sperm following increased sperm competition is likely to tradeoff against other male traits (Snook 2005), including other sperm traits (Moore et al 2004;Helfenstein et al 2008;Evans 2011;Immler et al 2011) as well as survival (Van Voorhies 1992). We applied a trade-off between s and μ to examine the potential interactions between sperm competition, allocation to different sperm traits and inbreeding depression in driving polyandry evolution, and to facilitate comparison with previous models that did not consider inbreeding, or resulting inbreeding depression in sperm traits (Engqvist 2012;Bocedi and Reid 2016).…”