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FIGURE 3 in Amphibians from Serra do Cipó, Minas Gerais, Brasil. VI: A New Species of the Physalemus deimaticus Group (Anura, Leptodactylidae)
FIGURE 3. Physalaemus claptoni sp. nov. (holotype UFMG 16784). Live adult male from Serra do Cipó, Municipality of Santana do Riacho, Minas Gerais, Brazil.
FIGURE 7 in Amphibians from Serra do Cipó, Minas Gerais, Brasil. VI: A New Species of the Physalemus deimaticus Group (Anura, Leptodactylidae)
FIGURE 7. Nuptial pads of (A) Physalaemus claptoni sp. nov. (paratype UFMG 5418), brown, not divided and (B) Physalaemus rupestris (topotype UFMG 13369), white cream, divided. Scale bar=5 mm.
Aligned DNA sequence matrix for phylogenetic analyses in the article "Fifty years after: a taxonomic revision of the amphibian species from the Ecuadorian biodiversity hotspot Abra de Zamora, with description of two new Pristimantis species"
<p>The aligned matrices are in fasta format. Genes are arranged as follows:</p> <p>Subgenus Huicundomantis (Huicundomantis.fas):</p> <p>12S = 1–905</p> <p>16S = 906–1820</p> <p>RAG-1 = 1821–2463</p> <p> </p> <p>Genus Lynchius (Lynchius.fas):</p> <p>12S = 1–1028</p> <p>16S = 1029–2313</p> <p>RAG-1 = 2314–2925</p> <p> </p> <p>Pristimantis orestes group (Pristimantis_orestes.fas):</p> <p>12S = 1–964</p> <p>16S = 965–2041</p> <p>RAG-1 = 2042–2683</p>
Data from: Sustained immune activation is associated with susceptibility to the amphibian chytrid fungus
The disease chytridiomycosis caused by the fungus Bd has devastated amphibian populations worldwide. Functional genomic contributions to host susceptibility remain enigmatic and vary between species and populations. We conducted experimental Bd infections in Rana yavapaiensis, a species with intraspecific variation in chytridiomycosis susceptibility, to assess the skin and spleen transcriptomic response to infection over time. We predicted that increased immune gene expression would be associated with a positive disease outcome, but we instead found that surviving frogs had significantly reduced immune gene expression compared to susceptible frogs and to uninfected controls. MHC class II gene expression was also significantly higher in susceptible frogs compared to surviving frogs. Furthermore, susceptible frogs expressed a significantly larger number of distinct class II alleles, demonstrating a negative correlation between class II expression, functional diversity, and survival. Expression of the MHC class II locus previously associated with Bd disease outcomes was a significant predictor of Bd infection intensity at early infection stages but not at late infection stages, suggesting initial MHC-linked immune processes are important for ultimate disease outcomes. We infer through disease association and phylogenetic analysis that certain MHC variants are linked to the immune expression that was negatively associated with survival, and we hypothesize that frogs that did not express these alleles could better survive infections. Our study finds that MHC expression at early and late infection stages predicts Bd infection intensity, and suggests that generating a sustained immune response against Bd may be counterproductive for surviving chytridiomycosis in this partially susceptible species.
FIGURE 4 in Quantifying vertebrate zoogeographical regions of Australia using geospatial turnover in the species composition of mammals, birds, reptiles and terrestrial amphibians
FIGURE 4. The zoogeographical regions proposed by Cracraft (1991, thick black lines) and superimposed over the three clusters found in this study.
Do epigenetic changes drive corticosterone responses to alarm cues in larvae of an invasive amphibian?
<p>The developmental environment can exert powerful effects on animal phenotype. Recently epigenetic modifications have emerged as one mechanism that can modulate developmentally plastic responses to environmental variability. For example, the DNA methylation profile at promoters of hormone receptor genes can affect their expression and patterns of hormone release. Across taxonomic groups, epigenetic alterations have been linked to changes in glucocorticoid (GC) physiology. GCs are metabolic hormones that influence growth, development, transitions between life-history stages, and thus fitness. To date, relatively few studies have examined epigenetic effects on phenotypic traits in wild animals, especially in amphibians. Here, we examined the effects of exposure to predation threat and experimentally manipulated DNA methylation on corticosterone (CORT) levels in tadpoles and metamorphs of the invasive cane toad (Rhinella marina). We included offspring of toads sampled from populations across the species' Australian range. In these animals, exposure to chemical cues from injured conspecifics induces shifts in developmental trajectories, putatively as an adaptive response that lessens vulnerability to predation. We exposed tadpoles to these alarm cues, and measured changes in DNA methylation and CORT levels, both of which are mechanisms that have been implicated in the control of phenotypically plastic responses in tadpoles. To test the idea that DNA methylation drives shifts in GC physiology, we also experimentally manipulated methylation levels with the drug zebularine. We found differentially methylated regions between control tadpoles and their full-siblings exposed to alarm cues, zebularine or both treatments. However, the effects of these manipulations on methylation patterns were weaker than clutch (e.g. genetic, maternal, etc.) effects. CORT levels were higher in larval cane toads exposed to alarm cues and zebularine. We found little evidence of changes in DNA methylation across the glucocorticoid receptor gene (NR3C1) promoter region in response to alarm cue or zebularine exposure. In both alarm cue and zebularine-exposed individuals, we found differentially methylated DNA in the suppressor of cytokine signaling 3 gene (SOCS3), which may be involved in predator avoidance behavior. In total, our data reveal that alarm cues have significant impacts on tadpole physiology, but show only weak links between DNA methylation and CORT levels. We also identify genes containing differentially methylated regions in tadpoles exposed to alarm cues and zebularine, particularly in range-edge populations, that warrant further investigation.</p>
Infection status as the basis for habitat choices in a wild amphibian
<p>Animals challenged with disease may select specific habitat conditions that help prevent or reduce infection. Whereas pre-infection avoidance of habitats with a high risk of disease exposure has been documented in both captive and free-ranging animals, evidence of post-infection habitat switching to conditions that promote the clearing of infection is limited to laboratory experiments. The extent to which wild animals proximately modify habitat choices in response to infection status therefore remains unclear. We investigated pre-infection behavioral avoidance and post-infection habitat switching using wild, radio-tracked boreal toads (<i>Anaxyrus boreas boreas</i>) in a population challenged with <i>Batrachochytrium dendrobatidis </i>(<i>Bd</i>); a pathogenic fungus responsible for a catastrophic panzootic affecting hundreds of amphibian species worldwide. <span>Boreal toads did not preemptively avoid microhabitats with conditions conducive to <i>Bd </i>growth. Infected individuals, however, selected warmer, more open habitats, </span>which were associated with elevated body temperature and the subsequent clearing of infection<span>. Our results suggest that disease </span>can comprise an important selective pressure on animal habitat and space use<span>. </span>Habitat selection models therefore may be greatly improved by including variables that quantify infection risk and/or the infection status of individuals through time.</p>
Scripts and files for "Small-scale population divergence is driven by local larval environment in a temperate amphibian"
<p>Genomic variation within and among populations is shaped by the interplay between natural selection and the effects of genetic drift and gene flow. Adaptive divergence can be found in small scale natural systems even when population sizes are small and the potential for gene flow is high, suggesting that local environments exert selection pressures strong enough to counteract the opposing effects of drift and gene flow. Here, we investigated genomic differentiation in nine moor frog (<i>Rana arvalis</i>) populations in a small-scale network of local wetlands using 16 707 ddRAD-seq SNPs, relating levels of differentiation with local environments as well as with properties of the surrounding landscape. We characterized population structure and differentiation, and partitioned the effects of geographic distance, local larval environment and landscape features on total genomic variation. We also conducted gene-environment association studies using univariate and multivariate approaches. We found small-scale population structure corresponding to 6-8 clusters. Local larval environment was the most influential component explaining 2.3% of the total genetic variation followed by landscape features (1.8%) and geographic distance (0.8%), indicative of isolation-by-environment, -by-landscape and -by-distance, respectively. We identified 1000 potential candidate SNPs putatively under divergent selection mediated by the local larval environment. The candidate SNPs were involved in, among other biological functions, immune system function and development. Our results suggest that small scale environmental differences can exert selection pressures strong enough to counteract homogenizing effects of gene flow and drift in this small-scale system leading to observable population differentiation.</p>
Adaptation to elevation but limited local adaptation in an amphibian
<p>We performed a reciprocal transplant experiment to estimate "parallel" adaptation to elevation and "unique" adaptation to local sites at the same elevation, using the frog <i>Rana temporaria</i> in the Swiss Alps. It is important to distinguish these two processes because they have different implications for population structure and ecological specialization. Larvae were reared from hatching to metamorphosis within enclosures installed in their pond of origin, in three foreign ponds at the same elevation, and in four ponds at different elevation (1500-2000 m higher or lower). There were two source populations from each elevation, and adults were held in a common environment for one year before they were crossed to produce offspring for the experiment. Fitness was a measure that integrated larval survival, development rate, and body size. Parallel adaptation to elevation was indicated by an advantage at the home elevation (11.5% fitness difference at low elevation and 47% at high elevation). This effect was stronger than that observed in most other studies, according to a survey of previous transplant experiments across elevation (<i>N</i> = 8 animal species and 71 plants). Unique local adaptation within elevational zones was only 0.3-0.7 times as strong as parallel adaptation, probably because gene flow is comparatively high among nearby wetlands at the same elevation. The home-elevation advantage may reduce gene flow across the elevational gradient and enable the evolution of habitat races specialized on elevation.</p>
Inter- and intraspecific variation in juvenile metabolism and water loss among five biphasic amphibian species
<p>Population persistence is informed by the ability of individuals to cope with local abiotic conditions, which is commonly mediated by physiological traits. Among biphasic amphibians, juveniles—which are infrequently studied but play a key role in amphibian population dynamics—are the first life stage to experience terrestrial conditions following the aquatic larval stage. To illuminate phenotypic variation that may allow juveniles to survive the physiological challenges presented by this transition, we examined respiratory surface area water loss (<i>RSAWL</i>) and standard metabolic rates (SMR) among juveniles reared under common larval conditions for five salamander species (<i>Ambystoma annulatum, A. maculatum, A. opacum, A. talpoideum, </i>and <i>A. texanum</i>) collected across ~200 km of latitude in Missouri, USA. We found that SMR described 34% of variation in <i>RSAWL</i>, suggesting that physiological water conservation may be limited by energetic regulation among these species, and vice versa<i>. </i>On average, species differed in juvenile SMR and residual values of <i>RSAWL</i> (corrected for body size/shape) by 0.04 mL CO<sub>2</sub><span><span> </span></span> and 0.16, respectively, possibly because of distinct species ecologies. For example, <i>A. annulatum </i>had higher SMR and <i>RSAWL</i> compared to broadly distributed study species, potentially associated with a relatively narrow range of environmental conditions experienced across the small geographic distribution of <i>A. annulatum</i>. Latitude correlated negatively with temperature and precipitation, and positively with <i>RSAWL, </i>suggesting that variation in <i>RSAWL</i> may be adaptive to local conditions. We provide evidence that species differences likely have a genetic basis, reflecting selection favoring species divergence to effectively use distinct microhabitats.</p>
Data from: Using automated digital recording systems as effective tools for the monitoring of birds and amphibians
There is a need to improve the quantity and quality of data in biodiversity monitoring projects. We compared an automated digital recording system (ADRS) with traditional methods (point-counts and transects) for the assessment of birds and amphibians. The ADRS proved to produce better quantity and quality of data. This new method has 3 additional advantages: permanent record of a census, 24 h/d data collection and the possibility of automated species identification.
A co-development approach to conservation leads to informed habitat design and rapid establishment of amphibian communities
<p>1. Effective wildlife restoration is a critical requirement of many conservation actions. The outcome of conservation interventions can be optimised through knowledge of species' habitat requirements, but few studies consider the impact of using explicit evidence from dedicated local research to inform the design phase of habitat management. Furthermore, interventions administered externally from the top down, whilst simpler than those developed in discussion with multiple stakeholders including land managers (i.e. co-development), run the risk of failing to engage local people.</p> <p>2. In this study, we focus on interventions in the Scottish Highlands to improve the availability and suitability of breeding ponds for local amphibian assemblages. We collected and analysed data based on 129 ecological variables across 88 reference ponds to quantify the local habitat preferences. We used the findings from these analyses to inform the construction or restoration of 25 intervention ponds co-developed in partnership with stakeholders (landowners, foresters, citizen scientists and government agencies). Following the interventions, we monitored amphibian communities at these sites over 4 years. We assessed presence and abundance of all five native amphibians (the anurans Rana temporaria and Bufo bufo, and the salamanders Lissotriton helveticus, L. vulgaris and Triturus cristatus) using egg searching, dip-netting, torching and trapping.</p> <p>3. The new habitats were overall characterised by ecological conditions more favourable to amphibians than the reference ponds. We recorded a total of 51 colonisation events. Within two breeding seasons after construction or restoration, the intervention ponds hosted the full complement of species, mirroring amphibian diversity patterns found in the local reference ponds.</p> <p>4. Our study shows that ecological research to quantify local habitat requirements and working with commercial land-managers to ensure equitable benefits prior to designing conservation actions can promote rapid and efficient recovery of wildlife.</p>
Data from: An identification of invariants in life history traits of amphibians and reptiles
<p>While many morphological, physiological, and ecological characteristics of organisms scale with body size, some do not change under size transformation. They are called invariant. A recent study recommended five criteria for identifying invariant traits. These are based on that a trait exhibits a unimodal central tendency and varies over a limited range with body mass (type I), or that it does not vary systematically with body mass (type II). We methodologically improved these criteria and then applied them to life history traits of amphibians, Anura, Caudata (eleven traits), and reptiles (eight traits). The numbers of invariant traits identified by criteria differed across amphibian orders and between amphibians and reptiles. Reproductive output (maximum number of reproductive events per year), incubation time, length of larval period, and metamorphosis size were type I and II invariant across amphibians. In both amphibian orders, reproductive output and metamorphosis size were type I and II invariant. In Anura, incubation time and length of larval period and in Caudata, incubation time were further type II invariant. In reptiles, however, only number of clutches per year was invariant (type II). All these differences could reflect that in reptiles body size and in amphibians, Anura, and Caudata metamorphosis (neotenic species go not through it) and the trend towards independence of egg and larval development from water additionally constrained life history evolution. We further demonstrate that all invariance criteria worked for amphibian and reptilian life history traits, although we corroborated some known and identified new limitations to their application.</p>
Data from: Unlocking the story in the swab: A new genotyping assay for the amphibian chytrid fungus Batrachochytrium dendrobatidis
One of the most devastating emerging pathogens of wildlife is the chytrid fungus, Batrachochytrium dendrobatidis (Bd), which affects hundreds of amphibian species around the world. Genomic data from pure Bd cultures has advanced our understanding of Bd phylogenetics, genomic architecture, and mechanisms of virulence. However pure cultures are laborious to obtain and whole genome sequencing is comparatively expensive, so relatively few isolates have been genetically characterized. Thus we still know little about the genetic diversity of Bd in natural systems. The most common non-invasive method of sampling Bd from natural populations is to swab amphibian skin. Hundreds of thousands of swabs have been collected from amphibians around the world, but Bd DNA collected via swabs is often low in quality and/or quantity. In this study, we developed a custom Bd genotyping assay using the Fluidigm Access Array platform to amplify 192 carefully-selected regions of the Bd genome. We obtained robust sequence data for pure Bd cultures and field-collected skin swabs. This new assay has the power to accurately discriminate among the major Bd clades, recovering the basic tree topology previously revealed using whole genome data. Additionally, we established a critical value for initial Bd load for swab samples (150 Bd genomic equivalents) above which our assay performs well. By leveraging advances in microfluidic multiplex PCR technology and the globally distributed resource of amphibian swab samples, non-invasive skin swabs can now be used to address critical spatial and temporal questions about Bd and its effects on declining amphibian populations.
Data from: Host species composition influences infection severity among amphibians in the absence of spillover transmission
Wildlife epidemiological outcomes can depend strongly on the composition of an ecological community, particularly when multiple host species are affected by the same pathogen. However, the relationship between host species richness and disease risk can vary with community context and with the degree of spillover transmission that occurs among co-occurring host species. We examined the degree to which host species composition influences infection by Batrachochytrium dendrobatidis (Bd), a widespread fungal pathogen associated with amphibian population declines around the world, and whether transmission occurs from one highly susceptible host species to other co-occurring host species. By manipulating larval assemblages of three sympatric amphibian species in the laboratory, we characterized the relationship between host species richness and infection severity, whether infection mediates growth and survivorship differently across various combinations of host species, and whether Bd is transmitted from experimentally inoculated tadpoles to uninfected tadpoles. We found evidence of a dilution effect where Bd infection severity was dramatically reduced in the most susceptible of the three host species (Anaxyrus boreas). Infection also mediated survival and growth of all three host species such that the presence of multiple host species had both positive (e.g., infection reduction) and negative (e.g., mortality) effects on focal species. However, we found no evidence that Bd infection is transmitted by this species. While these results demonstrate that host species richness as well as species identity underpin infection dynamics in this system, dilution is not the product of reduced transmission via fewer infectious individuals of a susceptible host species. We discuss various mechanisms, including encounter reduction and antagonistic interactions such as competition and opportunistic cannibalism that may act in concert to mediate patterns of infection severity, growth, and mortality observed in multihost communities.
Data from: Rapid diversification and time explain amphibian richness at different scales in the Tropical Andes, Earth's most biodiverse hotspot
The Tropical Andes are Earth's most species-rich biodiversity hotspot for both animals and plants. Nevertheless, the ecological and evolutionary processes underlying this extraordinary richness remain uncertain. Here, we examine the processes that generate high richness in the Andes relative to other regions in South America, and across different elevations within the Andes, using frogs as a model system. We combine distributional data, a newly generated time-calibrated phylogeny for 2318 frog species, and phylogenetic comparative methods to test the relative importance of diversification rates and colonization times for explaining Andean diversity at different scales. At larger scales (among regions and families), we find that faster diversification rates in Andean clades most likely explain high Andean richness. In contrast, at smaller temporal and spatial scales (within family-level clades, within the Andes), diversification rates rarely explain richness patterns. Instead, we show that colonization times are important for shaping elevational richness patterns within the Andes, with more species found in habitats colonized earlier. We suggest that these scale-dependent patterns might apply to many other richness gradients. Recognition of this scale-dependence may help to reconcile conflicting results among studies of richness patterns across habitats, regions, and organisms.
Data from: Effect of the landscape matrix on gene flow in a coastal amphibian metapopulation
Functional connectivity is crucial for the persistence of a metapopulation, because migration among subpopulations enables recolonization and counteracts genetic drift, which is especially important in small subpopulations. We studied the degree and drivers of connectivity among occupied patches of a coastal dune metapopulation of the Natterjack Toad (Epidalea calamita Laurenti), on the basis of microsatellite variation. As spatial landscape heterogeneity is expected to influence dispersal and genetic structure, we analyzed which landscape features affect functional connectivity and to what extent. Sixty different landscape resistance scenarios as well as the isolation-by-distance model were compared using two landscape genetics approaches. We identified three subpopulations with unidirectional levels of gene flow among the two most geographically separated subpopulations, while inferred gene flow into the geographically intermediate subpopulation was limited. Urbanization and vegetation height negatively affected connectivity. Low estimates of genetic diversity and effective population size indicate that conservation measures in the smallest and most isolated subpopulation are required.
Data from: Where have all the tadpoles gone? Individual genetic tracking of amphibian larvae until adulthood.
Reliably marking larvae and reidentifying them after metamorphosis is a challenge that has hampered studies on recruitment, dispersal, migration and survivorship of amphibians for a long time, as conventional tags are not reliably retained through metamorphosis. Molecular methods allow unique genetic fingerprints to be established for individuals. Although microsatellite markers have successfully been applied in mark–recapture studies on several animal species, they have never been previously used in amphibians to follow individuals across different life cycle stages. Here, we evaluate microsatellites for genetic across-stages mark–recapture studies in amphibians and test the suitability of available software packages for genotype matching. We sampled tadpoles of the dendrobatid frog Allobates femoralis, which we introduced on a river island in the Nature Reserve 'Les Nouragues' in French Guiana. In two subsequent recapture sessions, we searched for surviving juveniles and adults, respectively. All individuals were genotyped at 14 highly variable microsatellite loci, which yielded unique genetic fingerprints for all individuals. We found large differences in the identification success of the programs tested. The pairwise-relatedness-based approach, conducted with the programs kingroup or ML-Relate, performed best with our data set. Matching ventral patterns of juveniles and adult individuals acted as a control for the reliability of the genetic identification. Our results demonstrate that microsatellite markers are a highly powerful tool for studying amphibian populations on an individual basis. The ability to individually track amphibian tadpoles throughout metamorphosis until adulthood will be of substantial value for future studies on amphibian population ecology and evolution.
Data from: Humidity levels drive reproductive modes and phylogenetic diversity of amphibians in the Brazilian Atlantic Forest
AIM: The diversity of reproductive modes among amphibians provides a striking example of how differences in the biology of species furnish can provide important explanations for species distribution patterns on a broad scale. We hypothesized that sites with a higher humidity level will support more different modes of reproduction than drier sites and will consequently exhibit a higher phylogenetic diversity. Furthermore, we predict that if there is a gradient in the tolerance of reproductive modes to desiccation, there will be a nested pattern in the composition of reproductive modes among sites. LOCATION: Twenty-seven forest sites in the Brazilian Atlantic Forest. METHODS: Through a path analysis approach, we evaluated the direct and indirect effects of the humidity level on the number of reproductive modes as well as the relative importance of both variables on amphibian phylogenetic diversity. A nestedness analysis was used to quantify the extent to which the composition of both species and reproductive modes in drier sites correspond to non-random subsets of those in sites with higher annual precipitation. RESULTS: We found that the reproductive modes present in drier sites are non-random subsets of those present in sites with higher humidity levels. Because reproductive modes are phylogenetically conserved among amphibians, sites with a greater number of reproductive modes supported greater phylogenetic diversity. Sites with high precipitation throughout the year provided adequate environmental conditions for a larger number of reproductive modes, whereas sites with low precipitation and typical seasonal climates supported only those reproductive modes specialized to resist desiccation. MAIN CONCLUSIONS: Our results show that humidity-related variables are key environmental factors related to both the richness of reproductive modes and phylogenetic diversity. We hypothesized that the higher phylogenetic diversity found in moister sites reflects differences in the tolerance to desiccation among different reproductive modes. Given that reproductive modes are associated with susceptibility to desiccation, their incorporation into explanatory models may trigger a great advance in the understanding of the mechanisms regulating the species richness and composition of amphibian communities.
Data from: Multiple stressors and the cause of amphibian abnormalities
The repeated occurrence of abnormal amphibians in nature points to ecological imbalance, yet identifying causes of these abnormalities has proved complex. Multiple studies have linked amphibian abnormalities to chemically contaminated areas, but inference about causal mechanisms is lacking. Here we use a high incidence of abnormalities in Alaskan wood frogs to strengthen inference about the mechanism for these abnormalities. We suggest that limb abnormalities are caused by a combination of multiple stressors. Specifically, toxicants lead to increased predation, resulting in more injuries to developing limbs and subsequent developmental malformations. We evaluated a variety of putative causes of frog abnormalities at 21 wetlands on the Kenai National Wildlife Refuge, south-central Alaska, USA, between 2004 and 2006. Variables investigated were organic and inorganic contaminants, parasite infection, abundance of predatory invertebrates, UVB, and temperature. Logistic regression and model comparison using the Akaike information criterion (AIC) identified dragonflies and both organic and inorganic contaminants as predictors of the frequency of skeletal abnormalities. We suggest that both predators and contaminants alter ecosystem dynamics to increase the frequency of amphibian abnormalities in contaminated habitat. Future experiments should test the causal mechanisms by which toxicants and predators may interact to cause amphibian limb abnormalities.
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Allen Brain Atlas
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