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 extreme temperatures can cause sex reversal during early ontogeny (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 laboratory 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.

Sex-chromosome evolution in frogs: what role for sex-antagonistic genes?

“…Sex reversals and leaky GSD are now being documented in the several species for which sex-linked markers have been developed (e.g. Rana clamitans , [ 37 ]; Rana dalmatina , [ 38 ]). Additionally, Jeffries et al .…”

Do the Offspring of Sex Reversals Have Higher Sensitivity to Environmental Perturbations?

“…New evidence shows that in fish, heatwaves can induce lasting epigenetic changes in somatic and reproductive tissues [Anastasiadi et al, 2021]. Theoretical and modeling studies call for attention to the possible effects of climate change in vertebrates with TSD (studies in reptiles predominate), with different predictions depending upon the variable taken into consideration [Valenzuela et al, 2019;Cornejo-Páramo et al, 2020;Nemesházi et al, 2020;Schwanz et al, 2020].…”

Evolutionary and demographic consequences of temperature-induced masculinization under climate warming: the effects of mate choice

“…However, species that have genetic sex determination, where the sex chromosomes or other genetic elements trigger male or female sexual development, are not safe from climate-induced sex-ratio shifts either. Sex reversals, where genetically female individuals become phenotypic males or vice versa, have been observed in various ectothermic taxa including fish [3], amphibians [4][5][6][7], reptiles [8], and invertebrates [9]. With increasing interest in this topic, sex reversal has been demonstrated in a growing number of species, suggesting that this phenomenon may be widespread [8].…”

“…Because sex reversal is challenging to study empirically, and only in recent years has it started to draw attention from field biologists and behavioural ecologists, no empirical study has yet tested the role of temperature-induced sex-reversal in mating success. However, increasing evidence shows that sexreversed and normal individuals differ in morphology, physiology, and behaviour [7,[21][22][23], all of which may affect mate choice. Furthermore, the sex-chromosome genotype of sex-reversed individuals differs from that of normal individuals of the same phenotypic sex, so they can be distinguished on the basis of phenotypic traits linked to sex chromosomes.…”