Trade-offs between immunity and testosterone in male African ground squirrels

Abstract

The immunocompetence handicap hypothesis (ICHH) proposes that testosterone has both beneficial effects on male reproductive potential and negative effects by suppressing the immune system. However, support for the ICHH has been variable and an alternative hypothesis suggests that testosterone may be acting indirectly via cortisol to suppress immunity (the stress-linked ICHH). A third hypothesis is that increased energetic investment in immunity results in the suppression of testosterone. We tested these hypotheses in male Cape ground squirrels () through two separate manipulations: first, by triggering a strong immune response using a lipopolysaccharide (LPS) injection and, secondly, by increasing circulating testosterone using silastic testosterone implants. Responding to an immune challenge significantly reduced testosterone, supporting the immune suppression hypothesis, while increasing circulating testosterone had no effect on immunocompetence, body mass, ectoparasite abundances or cortisol levels, failing to support either the ICHH or stress-linked ICHH. Our results add to the increasing body of literature that challenges the ICHH, and we conclude that the trade-off between testosterone and immunity is mediated through immune activation and not through testosterone in male Cape ground squirrels. Being able to test the ICHH, stress-linked ICHH and immune suppression hypotheses in a free-ranging mammal gives us a unique opportunity to examine the mechanisms mediating this trade-off.

Pathogens Shape Sex Differences in Mammalian Aging

“…Hence, we may expect that males will develop stronger disease symptoms, resulting in a lower probability of survival, and consequently increased between-sex differences in lifespan in pathogen-rich environments. However, inconsistencies among studies of vertebrate species (e.g., Cape ground squirrels, Xerus inauris [23]) suggest that testosterone is not the whole story.…”

Male Bowhead Whale Reproductive Histories Inferred from Baleen Testosterone and Stable Isotopes

“…Such factors often include body condition, stress, a suite of numerous social effects (e.g., presence of females, success in gaining access to females, social cues from females, interactions with other males, experience, dominance), as well as individual personality differences, epigenetic effects, immune costs, alternative mating strategies, and more ( Reeder and Kramer 2005 ; Greiner et al. 2010 ; Muehlenbein and Watts 2010 ; O'Brien et al. 2018 ; Ball and Balthazart 2020 ; Kraus et al.…”

Investment of both essential fatty and amino acids to immunity varies depending on reproductive stage

“…Similarly, in female dung beetles ( Euoniticellus intermedius ), activation of the immune system causes resources to be diverted away from reproduction (Reaney & Knell, ). Immune activation also results in lower circulating levels of testosterone in male Cape ground squirrels ( Xerus inauris ; O'Brien, Waterman, Anderson, & Bennett, ), and in lower sperm‐swimming velocity in Great Tits ( Parus major ), impairing reproductive ability (Losdat, Richner, Blount, & Helfenstein, ). In iteroparous species, including U. stansburiana , reproductive costs of immune challenges may be observed in later clutches or litters rather than in the immediate reproductive event (e.g., Marzal et al, ), something we do not have the data to assess in the current study.…”