Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity

Bókony, Veronika; Újhegyi, Nikolett; Hamow, Kamirán Áron; Bosch, Jaime; Thumsová, Barbora; Vörös, Judit; Aspbury, Andrea S.; Gabor, Caitlin R.

doi:10.1016/j.scitotenv.2020.141896

Cited by 41 publications

(53 citation statements)

References 60 publications

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“…Nevertheless, we had the highest number of phenotypic male samples from the pond where this individual was captured (Figure S1), thus, finding a single sex reversal at this site is compatible with the idea of an existing but very low frequency of sex reversal in the studied common toad populations. This almost complete lack of sex reversal is surprising, because we found many EDCs in the studied ponds, with higher concentrations in anthropogenic areas, as published in earlier papers (Bókony et al, 2021(Bókony et al, , 2018. Furthermore, we found a considerable number of female-to-male sex-reversed agile frogs (Rana dalmatina) in some of these ponds in the same years (Figure S1; Nemesházi et al, 2020).…”

Section: Discussionsupporting

confidence: 74%

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

Nemesházi

Sramkó

Laczkó

et al. 2021

Preprint

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Anthropogenic environmental changes are affecting biodiversity and microevolution worldwide. Ectothermic vertebrates are especially vulnerable, since their sexual development can be disrupted by environmental changes, which can cause sex reversal, a mismatch between genetic and phenotypic sex, potentially leading to sex-ratio distortion and population decline. Despite these implications, we have scarce empirical knowledge on the incidence of sex reversal in nature. Populations in anthropogenic environments may experience sex reversal more frequently, or alternatively, they may adapt to resist sex reversal. To test these alternative hypotheses, we developed PCR-based genetic sex markers for the common toad (Bufo bufo). We assessed 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 estrogenic 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 17α- ethinylestradiol (EE2) during larval development, whereas no sex reversal occurred in response to 1 ng/L EE2 and a glyphosate-based herbicide with 3 µg/L or 3 mg/L 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 surprisingly low sex-reversal frequency in wild toads compared to other ectothermic vertebrates studied before might indicate idiosyncratic, potentially species-specific resistance to sex reversal.

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Section: Discussionsupporting

confidence: 74%

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

Nemesházi

Sramkó

Laczkó

et al. 2021

Preprint

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“…Anuran tadpoles are well-known to show high levels of phenotypic plasticity in swimming performance and underlying morphological traits in response to a variety of environmental factors (e.g., Loman and Claesson 2003;Relyea 2004;Hoverman et al 2005;Castaneda et al 2006;Whiles et al 2010;Gomez-Mestre et al 2013). Interestingly, Bókony et al (2021) demonstrated that urban tadpoles of common toads (Bufo bufo) showed higher baseline stress and a more efficient recovery to baseline levels compared to tadpoles from natural habitats, partly as a response to water pollutants. These differences disappeared, however, when individuals were raised in a common garden environment, suggesting that divergence in the efficacy of negative feedback is driven by phenotypic plasticity rather than microevolutionary change (Bókony et al 2021).…”

Section: Modelmentioning

confidence: 99%

“…Interestingly, Bókony et al (2021) demonstrated that urban tadpoles of common toads (Bufo bufo) showed higher baseline stress and a more efficient recovery to baseline levels compared to tadpoles from natural habitats, partly as a response to water pollutants. These differences disappeared, however, when individuals were raised in a common garden environment, suggesting that divergence in the efficacy of negative feedback is driven by phenotypic plasticity rather than microevolutionary change (Bókony et al 2021). Urban-exploitative and invasive species often express highly flexible generalist phenotypes that enable them to colonise new habitats such as cities (Rodewald and Gehrt 2014;Ducatez et al 2018;Franzén et al 2020;Palacio 2020) and phenotypic plasticity plays an important role in facilitating the success of a small number of highly abundant species in cities (reviewed in Lowry et al 2013;Rodewald and Gehrt 2014).…”

Section: Modelmentioning

confidence: 99%

Growing up in a new world: trait divergence between rural, urban, and invasive populations of an amphibian urban invader

Mühlenhaupt¹,

Baxter‐Gilbert²,

Makhubo³

et al. 2021

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Cities are focal points of introduction for invasive species. Urban evolution might facilitate the success of invasive species in recipient urban habitats. Here we test this hypothesis by rearing tadpoles of a successful amphibian urban coloniser and invader in a common garden environment. We compared growth rate, morphological traits, swimming performance, and developmental rate of guttural toad tadpoles (Sclerophrys gutturalis) from native rural, native urban, and non-native urban habitats. By measuring these traits across ontogeny, we were also able to compare divergence across different origins as the tadpoles develop. The tadpoles of non-native urban origin showed significantly slower developmental rate (e.g., the proportion of tadpoles reaching Gosner stage 31 or higher was lower at age 40 days) than tadpoles of native urban origin. Yet, tadpoles did not differ in growth rate or any morphological or performance trait examined, and none of these traits showed divergent ontogenetic changes between tadpoles of different origin. These findings suggest that prior adaptation to urban habitats in larval traits likely does not play an important role in facilitating the invasion success of guttural toads into other urban habitats. Instead, we suggest that evolutionary changes in larval traits after colonization (e.g., developmental rate), together with decoupling of other traits and phenotypic plasticity might explain how this species succeeded in colonising extra-limital urban habitats.

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“…One possibility is that phenotypic differences could be the result of developmental effects experienced during the tadpole stage, which may be habitat-dependent for their expression in tadpoles and are carried over and expressed during post-metamorphic stages. Tadpoles are well known to show high levels of plasticity in many traits as a response to different ecological factors (Richardson 2001 ; Relyea 2002 ; Van Buskirk 2002 ; Relyea 2004 ) and differences in stress response between urban, agricultural, and rural Common Toad ( Bufo bufo ) tadpoles are seen to be a result of phenotypic plasticity (Bókony et al 2021 ). Furthermore, more active, explorative, and bolder phenotypes in Lake Frog ( Pelophylax ridibundus ) tadpoles are seen to be carried over to the adult stage (Wilson and Krause 2012b ) and if these traits arise through plasticity, then variable environments would be required to trigger their expression.…”

Section: Discussionmentioning

confidence: 99%

No evidence for innate differences in tadpole behavior between natural, urbanized, and invasive populations

Mühlenhaupt

Baxter‐Gilbert

Makhubo

et al. 2022

Behav Ecol Sociobiol

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Animals are increasingly challenged to respond to novel or rapidly changing habitats due to urbanization and/or displacement outside their native range by humans. Behavioral differences, such as increased boldness (i.e., propensity for risk-taking), are often observed in animals persisting in novel environments; however, in many cases, it is unclear how these differences arise (e.g., through developmental plasticity or evolution) or when they arise (i.e., at what age or developmental stage). In the Guttural Toad ( Sclerophrys gutturalis ), adult urban toads from both native and invasive ranges are bolder than conspecifics in natural habitats. Here, we reared Guttural Toad tadpoles in a common garden experiment, and tested for innate differences in boldness across their development and between individuals whose parents and lineage came from rural-native, urban-native, and urban-invasive localities (i.e., origin populations). Tadpoles did not differ in their boldness or in how their boldness changed over ontogeny based on their origin populations. In general, tadpoles typically became less bold as they aged, irrespective of origin population. Our findings indicate that differences in boldness in free-living adult Guttural Toads are not innate in the tadpole stage and we discuss three possible mechanisms driving phenotypic divergence in adult boldness for the focus of future research: habitat-dependent developmental effects on tadpole behavior, decoupled evolution between the tadpole and adult stage, and/or behavioral flexibility, learning, or acclimatization during the adult stage. Significance statement To determine if animals can persist in urban areas or become invasive outside their native ranges, it is important to understand how they adapt to life in the city. Our study investigates if differences in boldness that have been found in adult Guttural Toads ( Sclerophrys gutturalis ) represent heritable differences that can also be found in early life stages by rearing tadpoles from eggs in a common garden experiment. We did not find any differences in boldness among tadpoles from rural-native, urban-native, and urban-invasive origin populations. Our findings suggest that differences in boldness are not innate and/or that boldness is a behavioral trait that is decoupled between the tadpole and the adult stage.

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Stressed tadpoles mount more efficient glucocorticoid negative feedback in anthropogenic habitats due to phenotypic plasticity

Cited by 41 publications

References 60 publications

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

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

Growing up in a new world: trait divergence between rural, urban, and invasive populations of an amphibian urban invader

No evidence for innate differences in tadpole behavior between natural, urbanized, and invasive populations

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