Metabolic costs of altered growth trajectories across life transitions in amphibians

Abstract

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.

Climate change and ageing in ectotherms

“…Guerra, Zenteno‐Savín, Maeda‐Martínez, Philipp, & Abele, 2012), amphibians (e.g. Burraco, Valdés, & Orizaola, 2020), and reptiles (e.g. Furtado‐Filho, Polcheira, Machado, Mourão, & Hermes‐Lima, 2007).…”

“…Heritability estimates for telomere length in animals range from 0.18 to >1 (reviewed in Dugdale & Richardson, 2018; Haussmann & Heidinger, 2015; Reichert et al., 2015), tending to be higher when measured earlier in life (Dugdale & Richardson, 2018). However, in ectotherms (in contrast to most endotherms), telomeres show signs of elongation after birth in several species (reptiles: Ujvari et al., 2017; fish: McLennan et al., 2018; amphibians: Burraco et al., 2020). This makes it far from straightforward to decide the point in ontogeny at which telomere length should be compared between parents and offspring.…”

Phenotypic Switching Resulting From Developmental Plasticity: Fixed or Reversible?

“…An extensive (but not exhaustive) meta-analysis identified these phenomena in 38 mammalian, 91 piscine, 39 avian and 30 arthropod species (Hector and Nakagawa, 2012). While not analyzed in this study, compensatory growth also occurs in amphibians and reptiles -e.g., Roark et al (2009) and Burraco et al (2019). Interestingly, the evolutionarily highly conserved nature of compensatory or catch-up growth suggests a high degree of biological significance.…”

Oxidative stress mediates rapid compensatory growth and its costs

“…Yet, as for fast life history in general, there is ongoing debate about the role of oxidative stress in shaping rapid growth and its costs (Christensen et al., 2016; Monaghan & Ozanne, 2018; Smith et al., 2016). While several studies showed compensatory growth to be associated with increased oxidative stress (but see Noguera, Lores, Alonso‐Alvarez, & Velando, 2011), this was mainly based on the levels of antioxidant enzymes (birds: Alonso‐Alvarez, Bertrand, Faivre, & Sorci, 2007; fish: Costantini et al., 2018; damselflies: De Block & Stoks, 2008; ladybirds: Xie et al., 2015; frogs: Burraco, Valdés, & Orizaola, 2020) and very rarely on the direct measurement of oxidative damage (fish: Kim, Noguera, & Velando, 2019; birds: Costantini et al., 2018). Therefore, current evidence is largely inconclusive because levels of antioxidant defence may covary both negatively as positively with oxidative damage (Costantini & Verhulst, 2009).…”