Copulation corrupts immunity: A mechanism for a cost of mating in insects

Abstract

There are well documented costs of mating in insects but little evidence for underlying mechanisms. Here, we provide experimental evidence for a hormone-based mechanism that reduces immunity as a result of mating. We examined the mealworm beetle Tenebrio molitor and show that (i) mating reduces a major humoral immune effector-system (phenoloxidase) in both sexes, and (ii) that this down-regulation is mediated by juvenile hormone. Because both juvenile hormone and phenoloxidase have highly conserved functions across all insects, the identified mechanism is similarly likely to be highly conserved. The positive physiological function of mating-induced juvenile hormone secretion is gamete and accessory gland production: we propose that its negative effects on immune function are the consequence of physiological antagonism. Therefore, we have identified a physiological tradeoff between mating and immunity. Our results suggest that increasing mating success can result in increasing periods of immune suppression, which in turn implies that reproductively successful individuals may be more vulnerable to infection by, and the negative fitness effects of, pathogens.

The cost of reproduction: the devil in the details

“…Recent evidence suggests that pleiotropic effects of JH link immune function and reproduction. In the fl our beetle Tenebrio molitor, mating was reported to cause immunosuppression (decreased phenoloxidase activity) by increasing the level of JH [39]. These results are consistent with the hypothesis that JH reduces immune function.…”

Interactions between injury, stress resistance, reproduction, and aging in Drosophila melanogaster

“…Mating is harmful to both genders; when the male injects the female with sperm, the male introduces a foreign substance to the female's body which elicits an immune response. Thus, in addition to making sperm, the male makes enzymes that protect the sperm from the female's immune response (Rolff and Siva-Jothy, 2002). …”

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

“…Responses to mating are predicted to be sex specific, and these differences can be attributed to the divergent reproductive roles of the sexes. For example, mating induces significant changes in female insects including: elevated egg‐laying rate, increased food consumption, reduced immunity, and reduced receptivity to courting males (Chapman, Liddle, Kalb, Wolfner, & Partridge, 1995; Liu & Kubli, 2003; Rolff & Siva‐Jothy, 2002; Sgrò, Chapman, & Partridge, 1998). Less is known about the responses to mating in males, although they are predicted to primarily involve the replenishment of sperm and seminal fluid storage (Sirot, Buehner, Fiumera, & Wolfner, 2009).…”