TY - JOUR

T1 - Novel genetic sex markers reveal unexpected lack of, and similar susceptibility to, sex reversal in free-living common toads in both natural and anthropogenic habitats

AU - Nemesházi, Edina

AU - Sramkó, Gábor

AU - Laczkó, Levente

AU - Balogh, Emese

AU - Szatmári, Lajos

AU - Vili, Nóra

AU - Ujhegyi, Nikolett

AU - Üveges, Bálint

AU - Bókony, Veronika

N1 - © 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

PY - 2022/4

Y1 - 2022/4

N2 - Anthropogenic environmental changes are affecting biodiversity and microevolution worldwide. Ectothermic vertebrates are especially vulnerable because environmental changes can disrupt their sexual development and cause sex reversal, a mismatch between genetic and phenotypic sex. This can potentially lead to sex-ratio distortion and population decline. Despite these implications, there is scarce empirical knowledge on the incidence of sex reversal in nature. Populations in anthropogenic environments may be exposed to sex-reversing stimuli more frequently, which may lead to higher sex-reversal rate or, alternatively, these populations may adapt to resist sex reversal. We developed PCR-based genetic sex markers for the common toad (Bufo bufo) to assess the prevalence of sex reversal in wild populations living in natural, agricultural and urban habitats, and the susceptibility of the same populations to two ubiquitous oestrogenic pollutants in a common garden experiment. We found negligible sex-reversal frequency in free-living adults despite the presence of various endocrine-disrupting pollutants in their breeding ponds. Individuals from different habitat types showed similar susceptibility to sex reversal in the laboratory: all genetic males developed female phenotype when exposed to 1 µg L -1 17α-ethinylestradiol (EE2) during larval development, whereas no sex reversal occurred in response to 1 ng L -1 EE2 and a glyphosate-based herbicide with 3 µg L -1 or 3 mg L -1 glyphosate. The latter results do not support that populations in anthropogenic habitats would have either increased propensity for or higher tolerance to chemically induced sex reversal. Thus, the extremely low sex-reversal frequency in wild toads compared to other ectothermic vertebrates studied before might indicate idiosyncratic, potentially species-specific resistance to sex reversal.

AB - Anthropogenic environmental changes are affecting biodiversity and microevolution worldwide. Ectothermic vertebrates are especially vulnerable because environmental changes can disrupt their sexual development and cause sex reversal, a mismatch between genetic and phenotypic sex. This can potentially lead to sex-ratio distortion and population decline. Despite these implications, there is scarce empirical knowledge on the incidence of sex reversal in nature. Populations in anthropogenic environments may be exposed to sex-reversing stimuli more frequently, which may lead to higher sex-reversal rate or, alternatively, these populations may adapt to resist sex reversal. We developed PCR-based genetic sex markers for the common toad (Bufo bufo) to assess the prevalence of sex reversal in wild populations living in natural, agricultural and urban habitats, and the susceptibility of the same populations to two ubiquitous oestrogenic pollutants in a common garden experiment. We found negligible sex-reversal frequency in free-living adults despite the presence of various endocrine-disrupting pollutants in their breeding ponds. Individuals from different habitat types showed similar susceptibility to sex reversal in the laboratory: all genetic males developed female phenotype when exposed to 1 µg L -1 17α-ethinylestradiol (EE2) during larval development, whereas no sex reversal occurred in response to 1 ng L -1 EE2 and a glyphosate-based herbicide with 3 µg L -1 or 3 mg L -1 glyphosate. The latter results do not support that populations in anthropogenic habitats would have either increased propensity for or higher tolerance to chemically induced sex reversal. Thus, the extremely low sex-reversal frequency in wild toads compared to other ectothermic vertebrates studied before might indicate idiosyncratic, potentially species-specific resistance to sex reversal.

KW - amphibians

KW - feminization

KW - human-induced environmental change

KW - molecular sex markers

KW - sex change

KW - sex-chromosome identification

U2 - 10.1111/mec.16388

DO - 10.1111/mec.16388

M3 - Article

C2 - 35146823

VL - 31

SP - 2032

EP - 2043

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 7

ER -