Decreased attractivity in female garter snakes treated with an aromatase inhibitor

Abstract

Most experimental studies on sexual signal regulation via hormone manipulation have focused on male signals, yet female signals demonstrate substantial phenotypic variation and hormone‐dependent expression. Female red‐sided garter snakes (Thamnophis sirtalis parietalis) produce a skin‐based sex pheromone used by males in mate selection. The principle female sex steroid, 17 β‐estradiol, controls pheromone production in snakes, but studies manipulating female garter snakes have produced conflicting results, relied on behavioral tests with males in the laboratory, and did not quantify pheromone expression. Because aromatase is the terminal enzyme in estradiol biosynthesis, we hypothesized that female garter snakes rely on aromatase to ultimately control pheromone production during the annual cycle of this species. To test this, we used a known pharmacological inhibitor of aromatase, fadrozole (FAD). Wild‐caught female garter snakes were chronically treated via subcutaneous injections of either FAD (1.0 mg kg−1) or saline (control) for six months in the laboratory during the active period of the annual cycle then hibernated. In two separate field bioassays the next spring at the den site, FAD females received approximately 50% less courtship from wild, sexually active male garter snakes compared to SHAM females. Pheromone analysis revealed that four of the largest, unsaturated methyl ketones were specifically downregulated in FAD females, indicating that aromatase action is a crucial, permissive step in the maintenance of female attractivity.

Reconsidering reproductive patterns in a model dissociated species, the red-sided garter snake: Sex-specific and seasonal changes in gonadal steroidogenic gene expression

“…If ovariectomized in spring, females have reduced attractivity the next spring ( 21 ). Systemic aromatase inhibition across the active year (spring to fall) reduces female pheromone production and attractivity the next spring ( 26 ). Further, male garter snakes given estradiol implants produce abundant female sex pheromone and are attractive to wild males, an effect lost once the implants are removed which indicates an activational role for estradiol ( 25 ).…”

“…Mating is not a requirement for ovarian recrudescence and parturition, though: females who do not mate in a given spring can still become gravid and give birth that year ( 22 , 24 ). Further, E 2 is crucial for regulating female reproduction in this species, such as vitellogenesis, receptivity, and attractivity/pheromone production ( 21 , 24 – 26 ). During the late summer, prior to dispersal back to the den, gametogenesis occurs in both sexes in preparation for the next spring ( 9 , 15 , 17 ).…”