“Heat waves” experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

Ujszegi, János; Bertalan, Réka; Újhegyi, Nikolett; Verebélyi, Viktória; Nemesházi, Edina; Mikó, Zsanett; Kásler, Andrea; Herczeg, Dávid; Szederkényi, Márk; Vili, Nóra; Gál, Zoltán; Hoffmann, Orsolya Ivett; Bókony, Veronika; Hettyey, Attila

doi:10.1016/j.scitotenv.2022.155297

Cited by 20 publications

(22 citation statements)

References 99 publications

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“…Altogether, we conclude that mortality and CORT-methodological issues might have added some noise to our data but, had there been a strong treatment effect, such an effect would have been unlikely to get masked by noise. Compared to the strong effect of a physiological stressor, heat exposure, which caused >90% sex reversal in previous experiments (Mikó et al, 2021;Ujszegi et al, 2022), the rates of sex reversal in the present study (11%-32%) were low. Therefore, the variation among treatment groups is probably attributable to random deaths combined with the low but steady "baseline" sex-reversal propensity in agile frogs (Bókony et al, 2021b;Ujszegi et al, 2022) rather than to a genuine effect of CORT treatment.…”

Section: Discussioncontrasting

confidence: 94%

“…Therefore, here we examined the role of corticosterone (CORT), the main glucocorticoid hormone of amphibians, in sex reversal in the agile frog ( Rana dalmatina Fitzinger, 1838). This anuran species has male‐heterogametic sex determination (XX/XY sex chromosomes) system (Jeffries et al, 2018), but larval heat stress causes female‐to‐male sex reversal (Mikó et al, 2021; Ujszegi et al, 2022), and ca. 20% of phenotypic males in natural populations are genetically females (Nemesházi et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

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Does stress make males? An experiment on the role of glucocorticoids in anuran sex reversal

Bókony,

Kalina,

Ujhegyi

et al. 2023

J Exp Zool Pt A

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Environmentally sensitive sex determination may help organisms adapt to environmental change but also makes them vulnerable to anthropogenic stressors, with diverse consequences for population dynamics and evolution. The mechanisms translating environmental stimuli to sex are controversial: although several fish experiments supported the mediator role of glucocorticoid hormones, results on some reptiles challenged it. We tested this hypothesis in amphibians by investigating the effect of corticosterone on sex determination in agile frogs (Rana dalmatina). This species is liable to environmental sex reversal whereby genetic females develop into phenotypic males. After exposing tadpoles during sex determination to waterborne corticosterone, the proportion of genetic females with testes or ovotestes increased from 11% to up to 32% at 3 out of 4 concentrations. These differences were not statistically significant except for the group treated with 10 nM corticosterone, and there was no monotonous dose‐effect relationship. These findings suggest that corticosterone is unlikely to mediate sex reversal in frogs. Unexpectedly, animals originating from urban habitats had higher sex‐reversal and corticosterone‐release rates, reduced body mass and development speed, and lower survival compared to individuals collected from woodland habitats. Thus, anthropogenic environments may affect both sex and fitness, and the underlying mechanisms may vary across ectothermic vertebrates.

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Section: Discussioncontrasting

confidence: 94%

Section: Introductionmentioning

confidence: 99%

Does stress make males? An experiment on the role of glucocorticoids in anuran sex reversal

Bókony,

Kalina,

Ujhegyi

et al. 2023

J Exp Zool Pt A

Self Cite

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“…For example, we recently found that sex ratio in the toad Bufo bufo (ZW/ZZ) was not affected by exposure to 30 • C, a temperature high enough to cause up to 100% female-to-male sex reversal in the frog Rana dalmatina (XX/XY) in the same experiment. [51] This contradicted the broadly cited study by Piquet, [53] where 25 • C produced male excess in Bufo vulgaris (a synonym for Bufo bufo). The contradiction can be resolved by realizing that Piquet captured her animals near Geneva, in a hybrid zone of Bufo bufo and Bufo spinosus, [78] two species that were thought to be one at the time.…”

Section: The Devil In the Details: How To Choose Suitable Methods?mentioning

confidence: 85%

“…[12] Detailed searching methods are described in Supplement 1, and the data extracted in Supplementary Table 1. We found only four experiments in which anuran species with both male and female heterogamety were studied for sex-reversal propensity, [22,[49][50][51] although heterogamety was not in their focus. Other studies were usually restricted to a single species.…”

Section: Experimental Evidence For ''Asymmetrical Sex Reversal''mentioning

confidence: 99%

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

Nemesházi

Bókony

2022

BioEssays

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Sex reversal, a mismatch between phenotypic and genetic sex, can be induced by chemical and thermal insults in ectotherms. Therefore, climate change and environmental pollution may increase sex-reversal frequency in wild populations, with wide-ranging implications for sex ratios, population dynamics, and the evolution of sex determination. We propose that reconsidering the half-century old theory "Witschi's rule" should facilitate understanding the differences between species in sex-reversal propensity and thereby predicting their vulnerability to anthropogenic environmental change. The idea is that sex reversal should be asymmetrical: more likely to occur in the homogametic sex, assuming that sex-reversed heterogametic individuals would produce new genotypes with reduced fitness. A review of the existing evidence shows that while sex reversal can be induced in both homogametic and heterogametic individuals, the latter seem to require stronger stimuli in several cases. We provide guidelines for future studies on sex reversal to facilitate data comparability and reliability.

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“…On day 20, we started thermal treatments as described in Ujszegi et al (2022) and monitored tadpoles daily to record any mortality events. We discarded dead individuals from further analysis because it is unknown how pathogen loads and their detectability change shortly after death of the host, and because of quick body decomposition at high temperatures preventing a precise necropsy.…”

Section: Methodsmentioning

confidence: 99%

Amphibian larvae benefit from a warm environment under simultaneous threat from chytridiomycosis and ranavirosis

Herczeg

Holly

Kásler

et al. 2023

Oikos

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Rising temperatures can facilitate epizootic outbreaks, but disease outbreaks may be suppressed if temperatures increase beyond the optimum of the pathogens while still within the temperature range that allows for effective immune function in hosts. The two most devastating pathogens of wild amphibians, Batrachochytrium dendrobatidis (Bd) and ranaviruses (Rv), co‐occur in large areas, yet little is known about the consequences of their co‐infection and how these consequences depend on temperature. Here we tested how exposure to Bd and subsequent exposure to Rv, followed by treatment at elevated temperatures (28 and 30°C versus 22°C) affected Bd and Rv prevalence, infection intensities, and resulting mortalities in larval agile frogs and common toads. We found multiple pieces of evidence that the presence of one pathogen influenced the prevalence and/or infection intensity of the other pathogen in both species, depending on temperature and initial Rv concentration. Generally, the 30°C treatment lowered the prevalence and infection intensity of both pathogens and, in agile frogs, this was mirrored by higher survival. These results suggest that if temperatures naturally increase or are artificially elevated beyond what is ideal for both Bd and Rv, amphibians may be able to control infections and survive even the simultaneous presence of their most dangerous pathogenic enemies.

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“Heat waves” experienced during larval life have species-specific consequences on life-history traits and sexual development in anuran amphibians

Cited by 20 publications

References 99 publications

Does stress make males? An experiment on the role of glucocorticoids in anuran sex reversal

Does stress make males? An experiment on the role of glucocorticoids in anuran sex reversal

Asymmetrical sex reversal: Does the type of heterogamety predict propensity for sex reversal?

Amphibian larvae benefit from a warm environment under simultaneous threat from chytridiomycosis and ranavirosis

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