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Phenotypic differences among species may evolve through genetic accommodation, but mechanisms accounting for this process are poorly understood. Here we compare hormonal variation underlying differences in the timing of metamorphosis among three spadefoot toads with different larval periods and responsiveness to pond drying. We find that, in response to pond drying, Pelobates cultripes and Spea multiplicata accelerate metamorphosis, increase standard metabolic rate (SMR), and elevate whole-body content of thyroid hormone (the primary morphogen controlling metamorphosis) and corticosterone (a stress hormone acting synergistically with thyroid hormone to accelerate metamorphosis). In contrast, Scaphiopus couchii has the shortest larval period, highest whole-body thyroid hormone and corticosterone content, and highest SMR, and these trait values are least affected by pond drying among the three species. Our findings support that the atypically rapid and canalized development of S. couchii evolved by genetic accommodation of endocrine pathways controlling metamorphosis, showing how phenotypic plasticity within species may evolve into trait variation among species. Genetic accommodation is a potential mechanism for the phenotypic divergence of species. Here, Kulkarni et al. compare endocrine responses of three spadefoot toad species to pond drying and suggest how evolution of mechanisms of developmental plasticity may account for trait variation among species.

The Sonoran Desert toad ( Incilius alvarius ) is the only animal known to secrete the psychedelic compound 5-MeO-DMT as a chemical defense, but the source of 5-MeO-DMT in I. alvarius remains unknown. Some amphibians produce chemical defenses endogenously or through symbiotic interactions, while others acquire them from specialized diets. In this study we analyzed toxin gland secretions and diet profiles from wild I. alvarius and sympatric anurans from native and urban habitats around Tucson, Arizona to explore possible links between diet and 5-MeO-DMT production. All I. alvarius secreted high concentrations of 5-MeO-DMT, whereas other sympatric toads did not. The diet of I. alvarius was similar to that of sympatric anurans, indicating that I. alvarius does not exhibit relative dietary specialization. We found slight dietary differences between I. alvarius in native and urbanized habitats. Taken together, these lines of evidence suggest that diet is not directly linked to 5-MeO-DMT production and support the alternative hypotheses that I. alvarius synthesizes 5-MeO-DMT endogenously or via a microbial symbiont.

The pathogenic chytrid fungus Batrachochytrium dendrobatidis (Bd) can cause precipitous population declines in its amphibian hosts. Responses of individuals to infection vary greatly with the capacity of their immune system to respond to the pathogen. We used a combination of comparative and experimental approaches to identify major histocompatibility complex class II (MHC-II) alleles encoding molecules that foster the survival of Bd-infected amphibians. We found that Bd-resistant amphibians across four continents share common amino acids in three binding pockets of the MHC-II antigen-binding groove. Moreover, strong signals of selection acting on these specific sites were evident among all species co-existing with the pathogen. In the laboratory, we experimentally inoculated Australian tree frogs with Bd to test how each binding pocket conformation influences disease resistance. Only the conformation of MHC-II pocket 9 of surviving subjects matched those of Bd-resistant species. This MHC-II conformation thus may determine amphibian resistance to Bd, although other MHC-II binding pockets also may contribute to resistance. Rescuing amphibian biodiversity will depend on our understanding of amphibian immune defence mechanisms against Bd. The identification of adaptive genetic markers for Bd resistance represents an important step forward towards that goal.

Organisms react to environmental changes through plastic responses that often involve physiological alterations with the potential to modify life-history traits and fitness. Environmentally induced shifts in growth and development in species with complex life cycles determine the timing of transitions between subsequent life stages, as well as body condition at transformation, which greatly determine survival at later stages. Here we show that spadefoot toad larvae surviving pond drying and predators experienced marked alterations in growth and development, and in their fat reserves, oxidative stress, and relative telomere length. Tadpoles accelerated development but reduced growth and consumed more fat reserves when facing pond drying. However, oxidative stress was buffered by increased antioxidant enzyme activity, and telomeres remained unchanged. Predators caused opposite effects: they reduced larval density, hence relaxing competition and allowing faster development and enhanced growth of survivors. Tadpoles surviving predators metamorphosed bigger and had larger fat bodies, increasing their short-term survival odds, but showed signs of oxidative stress and had shorter telomeres. Developmental acceleration and enhanced growth thus seemed to have different physiological consequences: reduced fat bodies and body size compromise short-term survival, but are reversible in the long run, whereas telomere shortening is non-reversible and could reduce long-term survival.

Resilience in amphibians lies in their ecological adaptability, driven by their genetic makeup. Eleutherodactylus coqui , native to Puerto Rico (PR) and a beloved symbol there, is among the most successful invasive amphibians. This species is extensively studied in terms of its biology and genetics, including being the first Eleutherodactylus with a draft genome. Its potential to spread to new habitats and rapid breeding are notable. Transcriptome analyses of E. coqui are limited but provide insights into their invasiveness and differential gene expression. We compared the skin transcriptomes of E. coqui from PR (native) to those from an area under citric acid treatment in Los Angeles, California (invasive) population. Our results show differences in stress response gene signatures between both populations. In the native population, we hypothesize these responses are due to immunity against diverse parasites, potentially helping control their native populations in PR. Additionally, these coquis expressed several antimicrobial peptides, which were previously reported to be absent in coquis. These peptides may play a role in the invasiveness of the common coqui and its tolerance to urban and degraded habitats. We also provide novel draft transcriptomes of close relatives of E. coqui : Eleutherodactylus planirostris , Eleutherodactylus johnstonei, Eleutherodactylus cochranae , and Pristimantis unistrigatus .

Exposure to stressors at formative stages in the development of wildlife and humans can have enduring effects on health. Understanding which, when and how stressors cause enduring health effects is crucial because these stressors might then be avoided or mitigated during formative stages to prevent lasting increases in disease susceptibility. Nevertheless, the impact of early-life exposure to stressors on the ability of hosts to resist and tolerate infections has yet to be thoroughly investigated. Here, we show that early-life, 6-day exposure to the herbicide atrazine (mean ± s.e.: 65.9±3.48 µg l−1) increased frog mortality 46 days after atrazine exposure (post-metamorphosis), but only when frogs were challenged with a chytrid fungus implicated in global amphibian declines. Previous atrazine exposure did not affect resistance of infection (fungal load). Rather, early-life exposure to atrazine altered growth and development, which resulted in exposure to chytrid at more susceptible developmental stages and sizes, and reduced tolerance of infection, elevating mortality risk at an equivalent fungal burden to frogs unexposed to atrazine. Moreover, there was no evidence of recovery from atrazine exposure. Hence, reducing early-life exposure of amphibians to atrazine could reduce lasting increases in the risk of mortality from a disease associated with worldwide amphibian declines. More generally, these findings highlight that a better understanding of how stressors cause enduring effects on disease susceptibility could facilitate disease prevention in wildlife and humans, an approach that is often more cost-effective and efficient than reactive medicine.

Animals that wield toxins face self-intoxication. Poison frogs have a diverse arsenal of defensive alkaloids that target the nervous system. Among them is epibatidine, a nicotinic acetylcholine receptor (nAChR) agonist that is lethal at microgram doses. Epibatidine shares a highly conserved binding site with acetylcholine, making it difficult to evolve resistance yet maintain nAChR function. Electrophysiological assays of human and frog nAChR revealed that one amino acid replacement, which evolved three times in poison frogs, decreased epibatidine sensitivity but at a cost of acetylcholine sensitivity. However, receptor functionality was rescued by additional amino acid replacements that differed among poison frog lineages. Our results demonstrate how resistance to agonist toxins can evolve and that such genetic changes propel organisms toward an adaptive peak of chemical defense.

Host defense peptides (HDPs) are a group of antimicrobial peptides (AMPs) that are crucial components of the innate immune system of many different organisms. These small peptides actively kill microbes and prevent infection. Despite the presence of AMPs in the amphibian immune system, populations of these organisms are in decline globally. Magainin is an AMP derived from the African clawed frog (Xenopus laevis) and has displayed potent antimicrobial effects against a wide variety of microbes. Included in this group of microbes are known pathogens of the African clawed frog and other amphibian species. Arguably, the most deleterious amphibious pathogen is Batrachochytrium dendrobatidis, a chytrid fungus. Investigating the mechanism of action of magainin can help understand how to effectively fight off infection. By understanding amphibian AMPs’ role in the frog, a potential conservation strategy can be developed for other species of amphibians that are susceptible to infections, such as the North American green frog (Rana clamitans). Considering that population declines of these organisms are occurring globally, this effort is crucial to protect not only these organisms but the ecosystems they inhabit as well.

Background Color and patterns in animals are closely tied to reproduction and survival, and have long been of interest to evolutionary biologists. For instance, bright conspicuous coloration plays a vital role in aposematic organisms as these phenotypes help communicate to potential predators that they are chemically defended and therefore unpalatable. Although the field has made significant progress in identifying genes associated with the production of conspicuous coloration, our knowledge of the genes associated with carotenoid metabolism and their roles in pigmentation is incomplete. Here we attempt to fill this knowledge gap by investigating how dietary carotenoid and retinol availability affects levels of gene expression and color formation in two color morphs of the mimic poison frog ( Ranitomeya imitator ), the orange-banded Sauce morph and the red-headed Varadero morph which exhibit bright orange and red coloration, respectively. Results We found that froglets raised under a carotenoid/retinol-enriched diet showed elevated expression levels of genes associated with the retinol pathway (e.g., dhrs3 , pnpla3 ) whereas froglets raised under a carotenoid/retinol-deficient diet showed elevated expression levels of genes associated with the retinoic acid pathway (e.g., aldh1l1 , aldh6a1 , cyp7a1 ). In addition, we found that froglets raised on a carotenoid/retinol-enriched diet displayed brighter skin and higher ratio of bright colored to black skin patches when compared to froglets raised on a carotenoid/retinol-deficient diet in both the Sauce and Varadero morph. Conclusions The genetic basis of carotenoid metabolism and its role in pigmentation remain poorly understood in amphibians. Our results provide insights into the key genes associated with carotenoid/retinol metabolism and their roles in pigmentation which should be investigated further and experimentally manipulated.

Background In response to seasonal cold and food shortage, the Xizang plateau frogs, Nanorana parkeri (Anura: Dicroglossidae), enter a reversible hypometabolic state where heart rate and oxygen consumption in skeletal muscle are strongly suppressed. However, the effect of winter hibernation on gene expression and metabolic profiling in these two tissues remains unknown. In the present study, we conducted transcriptomic and metabolomic analyses of heart and skeletal muscle from summer- and winter-collected N. parkeri to explore mechanisms involved in seasonal hibernation. Results We identified 2407 differentially expressed genes (DEGs) in heart and 2938 DEGs in skeletal muscle. Enrichment analysis showed that shared DEGs in both tissues were enriched mainly in translation and metabolic processes. Of these, the expression of genes functionally categorized as “response to stress”, “defense mechanisms”, or “muscle contraction” were particularly associated with hibernation. Metabolomic analysis identified 24 and 22 differentially expressed metabolites (DEMs) in myocardium and skeletal muscle, respectively. In particular, pathway analysis showed that DEMs in myocardium were involved in the pentose phosphate pathway, glycerolipid metabolism, pyruvate metabolism, citrate cycle (TCA cycle), and glycolysis/gluconeogenesis. By contrast, DEMs in skeletal muscle were mainly involved in amino acid metabolism. Conclusions In summary, natural adaptations of myocardium and skeletal muscle in hibernating N. parkeri involved transcriptional alterations in translation, stress response, protective mechanisms, and muscle contraction processes as well as metabolic remodeling. This study provides new insights into the transcriptional and metabolic adjustments that aid winter survival of high-altitude frogs N. parkeri .