Abstract
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.
Highlights
Adaptive developmental plasticity evolves in response to environmental heterogeneity when organisms can unambiguously perceive the environment through reliable cues, and there exists a cross-environmental trade-off such that no single phenotype can maximise fitness across environments [1,2]
Growth rate was lower for animals exposed to low water (F1,85 = 29.68, P < 0.0001), and juveniles emerging from the low water treatment had on average 5% shorter hind limbs (27.572 ± 0.398 mm in juveniles from low water vs. 29.045 ± 0.387 mm in juveniles from high water, adjusted means; F1,26 = 5.66, P = 0.025) (Figure 3)
Mechanisms of developmental acceleration Tadpoles of the Western spadefoot toad accelerated development by an average of 32% in response to decreased water levels in our experiment resulting in a shorter larval period by over 2 weeks (Figure 2), which is among the highest responses reported in the literature for anurans [4,54]
Summary
Adaptive developmental plasticity evolves in response to environmental heterogeneity when organisms can unambiguously perceive the environment through reliable cues, and there exists a cross-environmental trade-off such that no single phenotype can maximise fitness across environments [1,2]. Accelerated metamorphosis, cannot occur prior to achieving an apparent developmental threshold [15,16] This ability to adjust larval period to the local aquatic habitat quality and duration may have played a major role in allowing different populations and even species to adapt to widely divergent environments. Accelerated metamorphosis decreases size at first reproduction [32], challenges immune response of postmetamorphic individuals [33], and affects juvenile morphology, resulting in shorter-limbed metamorphs [6,34] Such fat burning and sustained physiological effort would be expected to alter the redox balance, greatly increasing the production of reactive oxygen species (ROS). We evaluated the oxidative stress caused by accelerated development measuring the activity of three antioxidant enzymes and a biochemical marker of oxidative damage
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