The Cost of Being Sexy: The long quest to understand male sexual traits, testosterone, and immunocompetence

The Cost of Being Sexy. Lesley Evans Ogden. BioScience, Volume 68, Issue 6, 1 January 1753, Pages 393–399, https://doi.org/10.1093/biosci/biy043

The long quest to understand male sexual traits, testosterone, and immunocompetence

Cape ground squirrels have captured Jane Waterman's fascination for the last 30 years. “They’re so cool,” effuses Waterman. Studying them in South Africa, where these beguiling, furry mammals breed year round, she has revealed a treasure trove of surprises. Extremely social, females live in family groups with their young. Males disperse from their family group at about 3 years old, joining bachelor groups. In these all-male groups, males sleep together, groom one another, and move together through the veld. Males have no dominance hierarchy and defend no territories, and it is rare to see any sort of aggressive behavior, explains Waterman. But on the day when a female enters estrus, which lasts about 3 hours, an average of 11 males show up to try to breed. Winners in this mating game are typically older, in better body condition, and “well endowed” with big testes and more sperm, she says. Big testes, theory holds, are usually supported with an abundance of testosterone. But Waterman has not found their testosterone levels higher than those in a lot of other less-endowed species.

This intrigued her. It seemed to Waterman that to support big testes, males had to be able to keep testosterone going year round. In these squirrels, she also found more ectoparasites on males than on females—not only when males are wide-ranging adults but also when they are homebody juveniles. Her hunch was that an influx of testosterone drives a reduced male ability to fend off ectoparasites, espousing an idea known as the immunocompetence handicap hypothesis (ICHH). It is a hypothesis that she, with a graduate student, has recently tested experimentally.

Waterman's test of the ICHH follows on the heels of hundreds of studies since the idea was first articulated in The American Naturalist by Ivar Folstad and Andrew Karter in 1992. The ICHH proposes that elaborate male ornaments or signs of vigor are mediated at least in part by testosterone but that testosterone is costly in terms of compromising immune function. The ICHH is an influential hypothesis tracing its lineage back to Darwin's first musings about the tail of the peacock, the antlers of deer, and other exaggerated male traits that could attract the attention of females but might be costly for survival. For scientists who had long thought about sexual selection from a theoretical standpoint, here was a potential mechanism to explain it. The duality of testosterone—sexy but costly—suggested authors Folstad and Karter, provides a cue to choosy females as to which males cope with this burden best.

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