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The role of phenotypic plasticity in reproductive colonization of land by frogs: urea excretion and mechanisms to prevent ammonia toxicity during terrestrial developmentMendez Narvaez, Javier 24 June 2022 (has links)
Phenotypic plasticity is hypothesized to facilitate colonization by enabling rapid adaptive responses to novel environments. The colonization of land exposed ancestrally aquatic animals to new ecological and physiological challenges, including toxic waste disposal in dry environments. The repeated evolution of terrestrial breeding in frogs creates opportunities to study developmental adaptations that may facilitate aquatic-to-terrestrial transitions. My dissertation examines the regulation of nitrogen excretion by early life stages in three anuran lineages that independently evolved terrestrial development. First, to assess developmental and environmentally cued changes, I measured N-waste accumulation over development in wet and dry environments in four species, then determined ammonia LC50 values to assess their risk of toxicity on land and the adaptive role of urea excretion. Ammonia accumulates developmentally in clutches or nests of all species and I found urea from both parental and embryonic larval sources. Embryonic larval urea excretion increased in response to dry conditions, and with ammonia accumulation, in the two species with longer terrestrial periods, and their urea excretion appears adaptive, preventing exposure to potentially lethal levels of ammonia. Where early life stages did not risk ammonia toxicity, they excreted no urea. Next, I examined biochemical mechanisms of ammonia detoxification. Urea excretion involves early onset of activity of two ornithine-urea cycle enzymes, arginase and carbamoyl phosphate synthetase, with regulatory plasticity in response to ammonia level during prolonged terrestriality and experimentally high aquatic ammonia. Glutamine synthetase activity provides another mechanism to detoxify ammonia during terrestrial development. Finally, I examined effects of prolonged terrestriality and the larval foam-making activity that supports it on larval physiology, development, and metamorphosis in Leptodactylus fragilis. Even young larvae effectively produced multiple foam nests. I found high ammonia concentrations in new larval nests, high urea excretion by developmentally arrested older larvae, and faster growth of larvae in water than while constructing nests. Larval foam-making extended terrestriality affected the aquatic larval period and age at metamorphosis, while metamorph size decreased with aquatic larval period, but increased with sibship size. Overall, my results suggest that, along with high ammonia tolerance, urea synthesis facilitates terrestrial development but carries physiological costs that may favor plasticity. Dehydration and ammonia accumulation are common, linked risks of terrestrial development. Along with parental adaptations, the evolved traits and plastic responses of early life stages are critical for transitions from aquatic to terrestrial breeding.
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