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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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  • Edina Nemesházi,
  • Zoltán Gál,
  • Nikolett Ujhegyi,
  • Viktória Verebélyi,
  • Zsanett Mikó,
  • Bálint Üveges,
  • Kinga Katalin Lefler,
  • Daniel L. Jeffries,
  • Orsolya Ivett Hoffmann,
  • Veronika BókonyOrcid
Edina Nemesházi
Hungarian Academy of Sciences Centre for Agricultural Research
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Zoltán Gál
National Agricultural Research and Innovation Centre
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Nikolett Ujhegyi
Hungarian Academy of Sciences Centre for Agricultural Research
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Viktória Verebélyi
Hungarian Academy of Sciences Centre for Agricultural Research
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Zsanett Mikó
Hungarian Academy of Sciences Centre for Agricultural Research
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Bálint Üveges
Hungarian Academy of Sciences Centre for Agricultural Research
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Kinga Katalin Lefler
Szent István Egyetem
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Daniel L. Jeffries
University of Lausanne
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Orsolya Ivett Hoffmann
National Agricultural Research and Innovation Centre
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Veronika Bókony
Orcid
Hungarian Academy of Sciences Centre for Agricultural Research
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Peer review status:IN REVISION

24 Apr 2020Submitted to Molecular Ecology
24 Apr 2020Assigned to Editor
24 Apr 2020Submission Checks Completed
20 May 2020Reviewer(s) Assigned
12 Jun 2020Review(s) Completed, Editorial Evaluation Pending
24 Jun 2020Editorial Decision: Revise Minor

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.