Condition-dependent SOD activity attenuates morph-specific superoxide effects on sperm performance

Abstract

Sperm competition theory predicts a negative correlation between somatic investment in traits that aid in pre- and postcopulatory sexual selection. Sperm performance is critical for postcopulatory success but are susceptible to damage by free radicals such as superoxide radicals generated during mitochondrial respiration (mtSOx). Males can ameliorate damage to spermatozoa by investing in the production of antioxidants, like superoxide dismutase (SOD), which may act as a mechanistic link for pre and postcopulatory trade-offs. Some male Australian, colour-polymorphic painted dragon lizards (Ctenophorus pictus) possess a yellow throat patch (bib) that females prefer over non-bibbed males and are also more likely to win male-male contests indicating that males with bibs are better at monopolizing females. We tested whether the sperm performance in non-bibbed males was superior to that of bibbed males as predicted by sperm competition theory. We show that blood cell mtSOx levels are negatively correlated with SOD activity in the plasma in all males early in the breeding season but SOD was lower in bibbed males. Non-bibbed males maintain a positive correlation between body condition and SOD activity over time while bibbed males do not. Overall sperm performance was not different between the bib-morphs, however, higher mtSOx levels were negatively correlated with sperm performance in bibbed males, but not of non-bibbed males. Together these data suggest physiological associations between body condition, SOD activity and sperm performance are linked to the expression of a yellow gular patch, which may be related to intrinsic differences in metabolism of bibbed versus non-bibbed males. Lay summaryDamage-inducing reactive oxygen species (ROS) are a by-product of oxygen-based energy production that are quenched by energetically expensive antioxidants. Male sexual colouration requires investment of energy and resources, which may constrain allocation to other functions like antioxidant production or spermatogenesis. Here we explored whether the body condition of colourful male lizards reflected their investment in antioxidants and reduction of ROS, which may influence sperm performance. We found that drab males in better condition had more antioxidants. Colourful males had lower levels of antioxidants and their sperm performed poorly at higher ROS levels. These results suggest a trade-off between colour maintenance and sperm performance.