Evolutionary reduction of developmental plasticity in desert spadefoot toads

Kulkarni, Saurabh S.; Gómez-Mestre, Iván; Moskalik, Christine L.; Storz, Brian L.; Buchholz, Daniel R.

doi:10.1111/j.1420-9101.2011.02370.x

Cited by 52 publications

(73 citation statements)

References 65 publications

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“…American spadefoot toads, for instance, have evolved a canalized accelerated larval development with respect to the slow but plastic development ancestral to the group as a result of their adaptation to ephemeral desert ponds [31]. Accelerated development has become nearly genetically assimilated, and plasticity has been lost to a great extent in desert spadefoot toads so they are no longer capable of long larval periods [31,64]. Such translation of ancestral environmentally induced changes in development within populations into adaptive constitutive divergences among taxa is a clear path connecting micro-and macroevolution [2,7,31].…”

Section: Discussionmentioning

confidence: 99%

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation

Gómez-Mestre

Jovani

2013

Proc. R. Soc. B.

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An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.

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Section: Discussionmentioning

confidence: 99%

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation

Gómez-Mestre

Jovani

2013

Proc. R. Soc. B.

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“…Tadpoles at 257C may have been closer to their optimum temperature (from a physiological point of view) and consequently experienced higher growth and developmental rates than tadpoles at either 217 or 297C, hence increasing lipid peroxidation (by-product of fat degradation). However, tadpoles reared at 297C may have developed too quickly to even have time to accumulate fat (Kulkarni et al 2011), hence reducing the rate of lipid peroxidation. More detailed analysis of lipid consumption during the course of anuran development and in response to changes in developmental and growth rates is needed to clarify the observed nonlinear patterns in oxidative stress with varying temperature.…”

Section: Discussionmentioning

confidence: 99%

Physiological Stress Responses in Amphibian Larvae to Multiple Stressors Reveal Marked Anthropogenic Effects even below Lethal Levels

Burraco

Gómez-Mestre

2016

Physiological and Biochemical Zoology

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Natural and anthropogenic disturbances cause profound alterations in organisms, inducing physiological adjustments to avoid, reduce, or remedy the impact of disturbances. In vertebrates, the stress response is regulated via neuroendocrine pathways, including the hypothalamic-pituitary-interrenal axis that regulates the secretion of glucocorticoids. Glucocorticoids have cascading effects on multiple physiological pathways, affecting the metabolic rate, reactive oxygen species production, or immune system. Determining the extent to which natural and anthropogenic environmental factors induce stress responses in vertebrates is of great importance in ecology and conservation biology. Here we study the physiological stress response in spadefoot toad tadpoles (Pelobates cultripes) against three levels of a series of natural and anthropogenic stressors common to many aquatic systems: salinity (0, 6, and 9 ppt), herbicide (0, 1, and 2 mg/L acid equivalent of glyphosate), water acidity (pH 4.5, 7.0, and 9.5), predators (absent, native, and invasive), and temperature (217, 257, and 297C). The physiological stress response was assessed examining corticosterone levels, standard metabolic rate, activity of antioxidant enzymes, oxidative cellular damage in lipids, and immunological status. We found that common stressors substantially altered the physiological state of tadpoles. In particular, salinity and herbicides cause dramatic physiological changes in tadpoles. Moreover, tadpoles reduced corticosterone levels in the presence of natural predators but did not do so against invasive predators, indicating a lack of innate recognition. Corticosterone and the antioxidant enzyme glutathione reductase were the most sensitive parameters to stress in this study. Anthropogenic perturbations of aquatic systems pose serious threats to larval amphibians even at nonlethal concentrations, judging from the marked physiological stress responses generated, and reveal the importance of incorporating physiological information onto conservation, ecological, and evolutionary studies.

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“…At the level of physiology, developmental acceleration seems to be a rather costly effort consuming a large fraction of the fat bodies accumulated during larval growth and/or preventing their accumulation [28]. Furthermore, developmental acceleration reduces size at metamorphosis [8,28,29], which is a commonly observed major factor influencing juvenile survival [30,31].…”

Section: Introductionmentioning

confidence: 99%

Mechanisms and Consequences of Developmental Acceleration in Tadpoles Responding to Pond Drying

2013

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Many amphibian species exploit temporary or even ephemeral aquatic habitats for reproduction by maximising larval growth under benign conditions but accelerating development to rapidly undergo metamorphosis when at risk of desiccation from pond drying. Here we determine mechanisms enabling developmental acceleration in response to decreased water levels in western spadefoot toad tadpoles (Pelobates cultripes), a species with long larval periods and large size at metamorphosis but with a high degree of developmental plasticity. We found that P. cultripes tadpoles can shorten their larval period by an average of 30% in response to reduced water levels. We show that such developmental acceleration was achieved via increased endogenous levels of corticosterone and thyroid hormone, which act synergistically to achieve metamorphosis, and also by increased expression of the thyroid hormone receptor TRΒ, which increases tissue sensitivity and responsivity to thyroid hormone. However, developmental acceleration had morphological and physiological consequences. In addition to resulting in smaller juveniles with proportionately shorter limbs, tadpoles exposed to decreased water levels incurred oxidative stress, indicated by increased activity of the antioxidant enzymes catalase, superoxide dismutase, and gluthatione peroxidase. Such increases were apparently sufficient to neutralise the oxidative damage caused by presumed increased metabolic activity. Thus, developmental acceleration allows spadefoot toad tadpoles to evade drying ponds, but it comes at the expense of reduced size at metamorphosis and increased oxidative stress.

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Evolutionary reduction of developmental plasticity in desert spadefoot toads

Cited by 52 publications

References 65 publications

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation, population viability and genetic variation

Physiological Stress Responses in Amphibian Larvae to Multiple Stressors Reveal Marked Anthropogenic Effects even below Lethal Levels

Mechanisms and Consequences of Developmental Acceleration in Tadpoles Responding to Pond Drying

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