Novel genetic sex markers reveal high frequency of sex reversal in wild
populations of the agile frog (Rana dalmatina) associated with
anthropogenic land use
Abstract
Populations of ectothermic vertebrates are vulnerable to environmental
pollution and climate change because certain chemicals and high
temperature can cause sex reversal during their larval development (i.e.
genetically female individuals develop male phenotype or vice versa),
which may distort population sex ratios. However, we have troublingly
little information on sex reversals in natural populations, due to
unavailability of genetic sex markers. Here we developed a genetic
sexing method based on sex-linked single nucleotide polymorphism loci to
study the prevalence and fitness consequences of sex reversal in agile
frogs (Rana dalmatina). Out of 125 juveniles raised in laboratory
without exposure to sex-reversing stimuli, 6 showed male phenotype but
female genotype according to our markers. These individuals exhibited
several signs of poor physiological condition, suggesting stress-induced
sex reversal and inferior fitness prospects. Among 162 adults from 11
wild populations in North-Central Hungary, 20% of phenotypic males had
female genotype according to our markers. These individuals occurred
more frequently in areas of anthropogenic land use; this association was
attributable to agriculture and less strongly to urban land use.
Female-to-male sex-reversed adults had similar body mass as normal
males. We recorded no events of male-to-female sex reversal either in
the lab or in the wild. These results support recent suspicions that sex
reversal is widespread in nature, and suggest that human-induced
environmental changes may contribute to its pervasiveness. Furthermore,
our findings indicate that sex-reversal is associated with stress and
poor health in early life, but sex-reversed individuals surviving to
adulthood may participate in breeding.