Different effects of accelerated development and enhanced growth on oxidative stress and telomere shortening in amphibian larvae

Burraco, Pablo; Díaz‐Paniagua, Carmen; Gómez-Mestre, Iván

doi:10.1038/s41598-017-07201-z

Cited by 82 publications

(76 citation statements)

References 69 publications

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“…Pacific horned frogs showed one of the widest range of sizes at metamorphosis reported for any amphibian in their natural population, individuals differing by up to 100% in body size and 890% in body mass. This range is broader than previously reported intrapopulation variation in the literature [31,43]. Pond permanence [30], food availability [44], temperature [45] and presence of predators or competitors [46,47] are known to have a profound effect on individual metamorphosing size in anurans, and the interaction between various selective pressures can determine a large spectrum of sizes.…”

Section: Discussionmentioning

confidence: 73%

“…However, a higher than optimal growth rate comes at a fitness cost, reflected in decreased survival [37]. Along with ecological factors, such as increased exposure to predators and competitors because of prolonged foraging [38], several other components can contribute to the lower fitness associated with accelerated growth rates, amongst which a lower resistance to starvation because of intense metabolism and low lipid reserves [40], delayed ossification [41], depressed immunological function [42], or cellular oxidative stress [43]. Some of the intrinsic costs mentioned above might have contributed to the observed higher mortality in the froglets that had metamorphosed at a small size in our study.…”

Section: Discussionmentioning

confidence: 99%

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How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

et al. 2020

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Background: In species with complex life cycles, size at metamorphosis is a key life-history trait which reflects the complex interactions between costs and benefits of life in the aquatic and terrestrial environments. Whereas the effects of a deteriorating larval habitat (e.g. pond desiccation) on triggering an early metamorphosis have been extensively investigated in amphibians, the consequences of the resulting reduced size at metamorphosis on fitness in the post-metamorphic terrestrial stage remain poorly understood. We tested the hypothesis that a smaller size at metamorphosis negatively affects performance and survival in the ensuing terrestrial stage. Using as model a tropical amphibian (Ceratophrys stolzmanni) showing a large phenotypic plasticity in metamorphosing traits, we evaluated the effects of size at metamorphosis on fitness-related trophic and locomotor performance traits, as well as on growth and survival rates. Results:Our results support the hypothesis that a larger size at metamorphosis is correlated with better survival and performance. The survival rate of large metamorphosing individuals was 95%, compared to 60% for those completing metamorphosis at a small size. Locomotor performance and gape size were positively correlated with body size, larger animals being more mobile and capable to ingest larger prey. However, smaller individuals achieved higher growth rates, thus reducing the size gap. Conclusions:Overall, size at metamorphosis affected profoundly the chances of survival in the short term, but smaller surviving individuals partly compensated their initial disadvantages by increasing growth rates. BackgroundSpecies with complex life cycles, such as biphasic amphibians and insects, are able to exploit different ecological niches and optimize their life-history in discrete developmental stages [1,2]. The transition occurring at metamorphosis usually requires dramatic and irreversible morphological transformations, and is frequently accompanied by a complete change of the ecological niche [3,4]. Pond-breeding amphibians, which in their post-larval stages become terrestrial, represent ideal models to investigate the independence of pre-and postmetamorphic life-stages and the presence of carry-over effects from one stage to the other, affecting the overall fitness of individuals [5]. The most evident trade-off between the aquatic and terrestrial stages is reflected in body size at metamorphosis. When the aquatic larvae are confronted with unfavourable conditions, such as food shortage [6,7], high density [8], desiccation risk

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Section: Discussionmentioning

confidence: 73%

Section: Discussionmentioning

confidence: 99%

How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

et al. 2020

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“…Intense cellular oxidative stress often shortens telomeres; however, the levels of redox changes detected in larvae showing compensating growth responses may not be enough to produce DNA damages, be tissue‐dependent or even be only apparent later in life. Previous studies in amphibians found shorter telomeres in tadpoles surviving predators and maintaining high growth rates (Burraco, Díaz‐Paniagua, & Gomez‐Mestre, ), or in tadpoles developing faster against permanent desiccation risk (Burraco, Valdés, Johansson, & Gomez‐Mestre, ). The lack of telomere shortening observed in our study can be also a consequence of the life history of the R. temporaria population used in this experiment.…”

Section: Discussionmentioning

confidence: 91%

Metabolic costs of altered growth trajectories across life transitions in amphibians

Burraco

Valdés

Orizaola

2019

Journal of Animal Ecology

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Climate change is causing increases in temperature and in the frequency of extreme weather events. Under this scenario, organisms should maintain or develop strategies to cope with environmental fluctuations, such as the capacity to modify growth trajectories. However, altering growth can have negative consequences for organisms’ fitness. Here, we investigated the metabolic alterations induced by compensatory growth during the larval development of the common frog (Rana temporaria), quantifying changes in oxidative stress, corticosterone levels and telomere length. We induced compensatory growth responses by exposing frog embryos to cold conditions (i.e. a ‘false spring’ scenario), which cause a delay in hatching. Once hatched, we reared larvae at two different photoperiods (24:0, representing the natural photoperiod of larvae, and 18:6) to test also for the interactive effects of light on growth responses. Larvae experiencing delayed hatching showed fast compensatory responses and reached larger size at metamorphosis. Larvae shortened their developmental period in response to delayed hatching. Non‐permanent light conditions resulted in relaxed growth compared with larvae reared under permanent light conditions, which grew at their natural photoperiod and closer to their maximal rates. Growth responses altered the redox status and corticosterone levels of larvae. These physiological changes were developmental stage‐dependent and mainly affected by photoperiod conditions. At catch‐up, larvae reared at 18:6 light:dark cycles showed higher antioxidant activities and glucocorticoid secretion. On the contrary, larvae reared at 24:0 developed at higher rates without altering their oxidative status, likely an adaptation to grow under very restricting seasonal conditions at early life. At metamorphosis, compensatory responses induced higher cellular antioxidant activities probably caused by enhanced metabolism. Telomere length remained unaltered by experimental treatments but apparently tended to elongate across larval ontogeny, which would be a first evidence of telomere lengthening across metamorphosis. Under the forecasted increase in extreme climatic events, adjusting growth and developmental rates to the dynamics of environmental fluctuations may be essential for survival, but it can carry metabolic costs and affect later performance. Understanding the implications of such costs will be essential to properly estimate the impact of climate change on wild animals.

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“…We then measured female telomere length, offspring telomere length, and body size soon after birth. There is evidence that the predator presence or predation attempts can have an effect on telomere length of the exposed individuals (Burraco, Díaz-Paniagua, & Gomez-Mestre, 2017;Kärkkäinen et al, 2019;McLennan et al, 2016;Olsson, Pauliny, Wapstra, & Blomqvist, 2010), thus suggesting that both females and offspring telomere length will be affected. However, no study has experimentally investigated the effect of the perception of predation risk on both female and offspring telomere length.…”

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confidence: 99%

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

Monteforte

Cattelan

Morosinotto

et al. 2020

Ecology and Evolution

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The perception of predation risk could affect prey phenotype both within and between generations (via parental effects). The response to predation risk could involve modifications in physiology, morphology, and behavior and can ultimately affect long‐term fitness. Among the possible modifications mediated by the exposure to predation risk, telomere length could be a proxy for investigating the response to predation risk both within and between generations, as telomeres can be significantly affected by environmental stress. Maternal exposure to the perception of predation risk can affect a variety of offspring traits but the effect on offspring telomere length has never been experimentally tested. Using a live‐bearing fish, the guppy (Poecilia reticulata), we tested if the perceived risk of predation could affect the telomere length of adult females directly and that of their offspring with a balanced experimental setup that allowed us to control for both maternal and paternal contribution. We exposed female guppies to the perception of predation risk during gestation using a combination of both visual and chemical cues and we then measured female telomere length after the exposure period. Maternal effects mediated by the exposure to predation risk were measured on offspring telomere length and body size at birth. Contrary to our predictions, we did not find a significant effect of predation‐exposure neither on female nor on offspring telomere length, but females exposed to predation risk produced smaller offspring at birth. We discuss the possible explanations for our findings and advocate for further research on telomere dynamics in ectotherms.

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Different effects of accelerated development and enhanced growth on oxidative stress and telomere shortening in amphibian larvae

Cited by 82 publications

References 69 publications

How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

How to recover from a bad start: size at metamorphosis affects growth and survival in a tropical amphibian

Metabolic costs of altered growth trajectories across life transitions in amphibians

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

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