Ezenwa, Vanessa; LaVere, Ashley; Hamlin, Heather; Lowers, Russell; Parrott, Benjamin
When you think about animal courtship, you may picture an ostentatious male strutting around to impress a group of females, like a peacock displaying its tail feathers; or two males fighting for a female’s favor, like two rams butting heads to show their strength. Although elaborate displays and acts of aggression may help a male win over females, success can have a downside. This is because testosterone, a key hormone supporting the development of courtship-related traits in males, can simultaneously suppress the immune system. As a result, the most successful males, in a courtship context, may be least successful at defending themselves against pathogens.
American alligators (Alligator mississippiensis) are large reptiles that live in freshwater coastal habitats across the southeastern United States. Compared to other reptiles, alligators have particularly strong immune systems, a possible adaptation to their pathogen-rich environment. However, during the breeding season, dominant males engage in aggressive, testosterone-fueled fights to win females. This raised the question of whether high testosterone males are more vulnerable to pathogens, or whether males have other physiological ways to overcome the negative effects of testosterone. It is also possible that external conditions, like temperature, could help modulate these negative effects. To address these questions, we studied the relationship between testosterone level and immune system potency in male alligators, including how temperature and co-circulating levels of another hormone, dehydroepiandrosterone (DHEA), affect the testosterone-immunity relationship.
We measured immune potency by quantifying the ability of alligator blood to kill three different pathogenic bacteria that alligators likely encounter in the wild. We found that bacteria killing by male alligators was best explained when testosterone levels were adjusted for DHEA levels. This suggests that co-circulating DHEA may help males manage the immunosuppressive effects of testosterone. We also found that by changing the temperature at which alligator blood had to fight bacteria, we changed the relationship between testosterone and immune potency. For some bacteria, testosterone affected bacteria killing only under cool temperatures, suggesting that external environmental conditions also determine the magnitude testosterone immunosuppression. Overall, our study shows that context is key to understanding how the male immune system responds to testosterone and that sometimes males can break even.