Does the spatial sorting of dispersal traits affect the phenotype of the non-dispersing stages of the invasive frog<i>Xenopus laevis</i>through coupling?

Kruger, Natasha; Measey, John; Vimercati, Giovanni; Herrel, Anthony; Secondi, Jean

doi:10.1093/biolinnean/blaa191

Cited by 6 publications

(7 citation statements)

References 78 publications

(109 reference statements)

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“…Yet, our study suggests that any adult body size differences are not driven by innate differences in tadpole growth rate, and it is unclear how they arose in adults (e.g., due to environmental factors such as food, due to phenotypic plasticity or due to directional selection for smaller or larger adult body sizes). In another successful amphibian invader, the African clawed frog (Xenopus laevis), Kruger et al (2021) showed that despite differences in adult body sizes between the core and periphery of the species' invasive distribution in France, the tadpoles did not show significant differences in growth rates when raised in a common garden experiment, indicating the decoupling of traits between life stages (but see Phillips 2009 for coupling of growth rate across larval and juvenile stages in cane toads, Rhinella marina). The decoupling of traits might also be a potential driver for the apparent similarities in growth rates of guttural toad tadpoles.…”

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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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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“…the one with the lowest AIC, is indicated in bold. ( Kruger et al, 2021). It remains to be tested whether adaptive shifts in tadpole optimum performance temperatures observed in this study are reflected in adult X. laevis.…”

Section: Discussionmentioning

confidence: 86%

Progeny ofXenopus laevisfrom altitudinal extremes display adaptive physiological performance

Wagener

Kruger

Measey

2021

Journal of Experimental Biology

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Environmental temperature variation generates adaptive phenotypic differentiation in widespread populations. We used a common garden experiment to determine whether offspring with varying parental origins display adaptive phenotypic variation related to different thermal conditions experienced in parental environments. We compared burst swimming performance and critical thermal limits of African clawed frog (Xenopus laevis) tadpoles bred from adults captured at high (∼ 2000 m above sea level) and low (∼ 5 m above sea level) altitudes. Maternal origin significantly affected swimming performance. Optimal swimming performance temperature had a >9°C difference between tadpoles with low altitude maternal origins (Topt: pure- and cross-bred 35.0°C) and high altitude maternal origins (Topt: pure-bred 25.5°C, cross-bred 25.9°C). Parental origin significantly affected critical thermal limits. Pure-bred tadpoles with low altitude parental origins had higher CTmax (37.8±0.8°C) than pure-bred tadpoles with high altitude parental origins and all cross-bred tadpoles (37.0±0.8 and 37.1±0.8°C). Pure-bred tadpoles with low altitude parental origins and all cross-bred tadpoles had higher CTmin (4.2±0.7 and 4.2±0.7°C) than pure-bred tadpoles with high altitude parental origins (2.5±0.6°C). Our study shows Xenopus laevis tadpoles’ varying thermal physiological traits is the result of adaptive responses to their parental thermal environments. This study is one of few demonstrating potential intraspecific evolution of critical thermal limits in a vertebrate species. Multi-generation common garden experiments and genetic analyses would be required to further tease apart the relative contribution of plastic and genetic effects to the adaptive phenotypic variation observed in these tadpoles.

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“…Conversely, differential expression of boldness between adults but not tadpoles might be the result of decoupled evolution between life stages in Guttural Toads (Collet and Fellous 2019 ). Decoupling of traits has recently been shown in the invasive African Clawed Frog ( Xenopus laevis ; Kruger et al 2021 ). Adults from the periphery of the invasive range in France show a distinct dispersal-mediating phenotype compared to adults from the core (Louppe et al 2018 ; Padilla et al 2019 ).…”

Section: Discussionmentioning

confidence: 99%

“…Adults from the periphery of the invasive range in France show a distinct dispersal-mediating phenotype compared to adults from the core (Louppe et al 2018 ; Padilla et al 2019 ). However, when reared from the egg to the post-metamorphic frog, those differences were not apparent, indicating that differences in adult traits emerge well after metamorphosis (Kruger et al 2021 ). Similarly, in a previous study, we presented data indicating that adult Guttural Toads are larger in urban areas but did not find differences in growth rates of tadpoles when raised in a common garden environment (Mühlenhaupt et al 2021 ).…”

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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Does the spatial sorting of dispersal traits affect the phenotype of the non-dispersing stages of the invasive frogXenopus laevisthrough coupling?

Cited by 6 publications

References 78 publications

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

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

Progeny ofXenopus laevisfrom altitudinal extremes display adaptive physiological performance

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

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