Immune Activation Reshapes Male Reproductive Investment and Induces Intergenerational Effects on Offspring.

Abstract

The activation of the immune system is a major physiological challenge that can compromise reproductive investment in males. While its effects on visual sexual signals have been widely investigated, much less is known about how immune activation influences acoustic signaling and other key reproductive traits. In this context, traits such as sperm production and sperm oxidative status (i.e., the balance between antioxidant and pro-oxidant molecules that ultimately determines the level of damage accumulation) are especially relevant, as they may potentially affect not only male fertility but also offspring development and behavior. Here, by experimentally activating the immune system of male field crickets (Gryllus bimaculatus) with a nylon monofilament (i.e., a non-pathogenic immune elicitor), we show that our immune treatment decreased male investment in acoustic sexual signaling, but had no effects on sperm production or sperm oxidative status (i.e., antioxidants and protein oxidative damage levels). However, the eggs fertilized by immune-challenged males showed higher hatching success than those of control (immune-unchallenged) males. Moreover, after hatching, the nymphs sired by immune-challenged males exhibited altered behavioral development, displaying increased locomotor activity and exploratory behavior. These findings suggest that immune activation does not impose uniform costs across pre- and post-copulatory sexually selected traits. Instead, they suggest that when facing an immune challenge, males may strategically prioritize fertility success over sexual attractiveness and mate attraction. Importantly, our results reveal that such shifts extend beyond the male's own reproductive investment to influence offspring behavioral phenotypes, highlighting a previously underappreciated pathway linking immunity to intergenerational behavioral variation.