Dietary antioxidants, but not courtship effort, affect oxidative balance in the testes and muscles of crickets

Abstract

Recent interest has focused on the role of reactive oxygen species (ROS) as universal constraints in life-history evolution. Empirical studies have examined the oxidative costs of reproduction for females, with little work conducted on males. The male germline is thought to be particularly susceptible to oxidative damage because the testes, and the sperm themselves, can be prolific producers of ROS. We tested the hypothesis that protection of the male germline from oxidative damage represents a cost of reproduction for males. We fed male crickets, , with one of two experimental diets in which we manipulated the availability of dietary antioxidants, and we induced variation in their expenditure on courtship effort by manipulating access to females. We measured the total antioxidant capacity, levels of ROS production and the amount of oxidative damage to proteins in both testis and thoracic muscle tissues. Dietary antioxidants contributed to positive oxidative balance in both tissue types. Although the testes had greater antioxidant defences than muscle tissue, they also produced considerably higher levels of ROS and sustained higher levels of oxidative damage. Courtship effort had no impact on any measure of oxidative balance. Our data confirm that the male germline is especially susceptible to oxidative stress and that dietary antioxidants can alleviate this oxidative cost of reproduction.

The role of oxidative stress in postcopulatory selection

“…What constitutes high sperm 'performance' or 'quality' is dependent on species and mating context, but sperm velocity, motility, viability and longevity are predicted to be linked to male competitive reproductive success [43]. The production of more sperm requires increased cell divisions and metabolic activity in the testes [44], which may be accompanied by an increase in ROS production [45,46]. Even in relatively monogamous species with short-term sperm storage, such as humans [47], oxidative damage of sperm strongly influences fertilization and male reproductive success [48].…”

“…In response to selection from ROS damage, testicular tissues may have more antioxidant defence than other tissues [58,59] and are ubiquitous components of seminal fluid across taxa: insects [60], birds [56], fish [61] and mammals [50]. For example, the testes of the Pacific cricket, Teleogryllus oceanicus, a species in which sperm viability, rather than the number sperm, most strongly influences paternity [62], has 3× the ROS levels and 1.4× the antioxidant capacity of muscle tissues used for courtship displays; nevertheless, the testes still had 2.5× more protein damage than muscle [46]. The effect of seminal antioxidation is clearly demonstrated when human sperm cells are washed free of seminal plasma-without their antioxidant cocktail, they rapidly undergo ROS-linked DNA damage (reviewed in [4]).…”

Dietary antioxidants reduce damage and rescue sperm viability and fertility following oxidative stress in Drosophila melanogaster

“…This non‐specificity, is usually combated by the use of a multi‐pronged antioxidant system (Surai, 2002), which functions as a ROS‐scavenging mechanism. Antioxidant enzymes such as superoxide dismutase, catalase, and glutathione peroxidase, as well as non‐enzymatic mechanisms that involve antioxidants from the diet such as flavonoids, carotenoids, and vitamins E and C, help counter this oxidative damage (Simmons et al, 2018). In this study, we use two well‐studied dietary antioxidants, melatonin and lipoic acid, paired with a ROS‐inducer, paraquat, to physiologically assess the oxidative costs of reproduction in Drosophila melanogaster Meigen (Diptera: Drosophilidae) pre‐ and post‐copulation.…”

“…Several studies suggest ROS are critical factors in mediating reproductive trade‐offs (Simmons et al, 2018). For example, in D. melanogaster and zebra finches, Taeniopygia guttata (Vieillot), there are direct correlations between increased reproductive effort and increased susceptibility to oxidative stress (Salmon et al, 2001; Alonso‐Alvarez et al, 2004; Simmons et al, 2018). Interestingly, due to the high cost of gamete production in females, most studies have focused primarily on oxidative costs and their trade‐offs on reproduction in females (Simmons et al, 2018).…”

“…Studies done on ROS and reproductive trade‐offs in males have been promising. For example, male crickets, Teleogryllus oceanicus (Le Guillou), show that the male germline is particularly prone to oxidative stress and that dietary antioxidants alleviate this oxidative cost of reproduction (Simmons et al, 2018). In addition, in male Drosophila , ROS has been seen to have more far‐reaching effects for molding the outcomes of reproduction and immunity by affecting gamete viability (Radhakrishnan & Fedorka, 2012).…”