Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use

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...

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Veröffentlicht in:Molecular ecology 2020-10, Vol.29 (19), p.3607-3621
Hauptverfasser: Nemesházi, Edina, Gál, Zoltán, Ujhegyi, Nikolett, Verebélyi, Viktória, Mikó, Zsanett, Üveges, Bálint, Lefler, Kinga Katalin, Jeffries, Daniel Lee, Hoffmann, Orsolya Ivett, Bókony, Veronika
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container_end_page 3621
container_issue 19
container_start_page 3607
container_title Molecular ecology
container_volume 29
creator Nemesházi, Edina
Gál, Zoltán
Ujhegyi, Nikolett
Verebélyi, Viktória
Mikó, Zsanett
Üveges, Bálint
Lefler, Kinga Katalin
Jeffries, Daniel Lee
Hoffmann, Orsolya Ivett
Bókony, Veronika
description 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.
doi_str_mv 10.1111/mec.15596
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subjects Adults
agricultural habitats
Amphibians
Anthropogenic factors
Body mass
Breeding
Climate change
Environmental changes
Fitness
Frogs
Gene polymorphism
genetic sex marker
Laboratories
Land use
Males
Markers
masculinization
Natural populations
Nucleotides
Ontogeny
Phenotypes
Polymorphism
Populations
Rana dalmatina
Reproductive fitness
Sex
Sex reversal
Sexing
Single-nucleotide polymorphism
Urban areas
urbanization
Vertebrates
title Novel genetic sex markers reveal high frequency of sex reversal in wild populations of the agile frog (Rana dalmatina) associated with anthropogenic land use
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