Seasonal sex steroids indicate reproductive costs associated with snake fungal disease

Emergent diseases may result in population declines by inducing mortality directly or through sublethal effects on host reproduction. Snake fungal disease (SFD) is an emerging threat to biodiversity, but the sublethal impacts of disease on host fitness are poorly characterized in snakes. The cryptic nature of most snakes makes direct assessment of the fitness consequences of SFD challenging. In such contexts, measurement sex steroids that correlate positively with seasonal reproductive investment may be useful in inferring the scope of disease impacts. To test the hypothesis that SFD is associated with reproductive suppression, we measured testosterone and estradiol in free-ranging pygmy rattlesnakes with varying clinical signs of SFD. We also used real-time PCR to validate the relationship between clinical signs and Ophidiomyces ophiodiicola (Oo) DNA presence on the skin. Infected males had lower testosterone compared to uninfected males during summer spermatogenesis and the fall breeding season. Infected females were less likely to have elevated estradiol compared to uninfected females during spring vitellogenesis. Approximately 85% of individuals with clinical signs were Oo DNA positive. Our findings are consistent with the hypothesis that coping with SFD comes at a cost to the reproductive success of afflicted individuals, and that seasonal sex steroids may be valuable early indicators of sublethal effects.