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Background Some dendrobatid poison frogs sequester the toxin epibatidine as a defense against predators. We previously identified an amino acid substitution (S108C) at a highly conserved site in a nicotinic acetylcholine receptor β2 subunit of dendrobatid frogs that decreases sensitivity to epibatidine in the brain-expressing α4β2 receptor. Introduction of S108C to the orthologous high-sensitivity human receptor similarly decreased sensitivity to epibatidine but also decreased sensitivity to acetylcholine, a potential cost if this were to occur in dendrobatids. This decrease in the acetylcholine sensitivity manifested as a biphasic acetylcholine concentration–response curve consistent with the addition of low-sensitivity receptors. Surprisingly, the addition of the β2 S108C into the α4β2 receptor of the dendrobatid Epipedobates anthonyi did not change acetylcholine sensitivity, appearing cost-free. We proposed that toxin-bearing dendrobatids may have additional amino acid substitutions protecting their receptors from alterations in acetylcholine sensitivity. To test this, in the current study, we compared the dendrobatid receptor to its homologs from two non-dendrobatid frogs. Results The introduction of S108C into the α4β2 receptors of two non-dendrobatid frogs also does not affect acetylcholine sensitivity suggesting no additional dendrobatid-specific substitutions. However, S108C decreased the magnitude of neurotransmitter-induced currents in Epipedobates and the non-dendrobatid frogs. We confirmed that decreased current resulted from fewer receptors in the plasma membrane in Epipedobates using radiolabeled antibodies against the receptors. To test whether S108C alteration of acetylcholine sensitivity in the human receptor was due to (1) adding low-sensitivity binding sites by changing stoichiometry or (2) converting existing high- to low-sensitivity binding sites with no stoichiometric alteration, we made concatenated α4β2 receptors in stoichiometry with only high-sensitivity sites. S108C substitutions decreased maximal current and number of immunolabeled receptors but no longer altered acetylcholine sensitivity. Conclusions The most parsimonious explanation of our current and previous work is that the S108C substitution renders the β2 subunit less efficient in assembling/trafficking, thereby decreasing the number of receptors in the plasma membrane. Thus, while β2 S108C protects dendrobatids against sequestered epibatidine, it incurs a potential physiological cost of disrupted α4β2 receptor function.

Dendrobatid poison frogs sequester alkaloids from an arthropod diet and use them in chemical defense. Alkaloid defenses vary considerably within and among species, with important consequences for the protection they can and do provide against microorganisms and predators. Most of this variation is attributed to differences in frog diet and prey availability, but emerging evidence also suggests that frogs differ in their physiological ability to sequester alkaloids. Epibatidines are one of the most geographically and phylogenetically restricted alkaloid classes in poison frogs, having been found naturally only in two genera of dendrobatids (Epipedobates and Ameerega) from Ecuador and northern Peru. To test the hypothesis that the ability to sequester epibatidine is confined to the lineages Epipedobates and Ameerega, we experimentally administered epibatidine to individuals of five species, representing three different lineages of dendrobatid poison frogs, including those known to possess (Epipedobates anthonyi) and lack (Ranitomeya variabilis, Ranitomeya imitator, Phyllobates vittatus, Dendrobates tinctorius) epibatidines in nature. All five species sequestered epibatidine; however, the percentage sequestered varied significantly across species with Epipedobates and Ranitomeya accumulating about 2.4× more than Phyllobates or Dendrobates. Our results suggest that the absence of epibatidine in certain dendrobatids is not due to the inability of these frogs to sequester epibatidine, but may instead result from differences in prey availability and/or dietary preference. Our finding of differences in the percentage of epibatidine sequestered among species points to the importance that physiological differences in sequestration play in explaining some of the alkaloid variation (including epibatidine) observed among dendrobatid poison frogs.

The poison frog family (Anura: Dendrobatidae) consists of species with conspicuous (e.g., warning coloration and toxicity or low palatability) and cryptic (e.g., palatable, and inconspicuous coloration) traits. Previous literature suggests that conspicuous, but not cryptic, species require diet specialization in prey high in alkaloids. To test for dietary preferences of poison frog species, we identified, to the lowest possible taxonomic rank, the diets of 21 Epipedobates darwinwallacei (conspicuous) and 22 Hyloxalus awa (cryptic) frogs living in syntopy in the Otongachi Forest in northwestern Ecuador. We then tested for differences in diet assemblage composition, and diet specialization, in these putatively conspicuous and cryptic frogs. Our analyses showed significant differences in the composition of arthropod assemblages consumed by both frog species, which translated into a narrow niche breadth and nine arthropod taxa (out of a total of 18) consumed by both species. Moreover, the index of relative importance, which measures frog’s diet specialization, suggested that E. darwinwallacei, and H. awa prefer specific arthropod taxa, where the former consumes preferentially springtails and mites, while the latter consumes mostly ants and Coleoptera larvae. Thus, contrary to expectations, diet specialization is not a unique characteristic of the species with conspicuous traits when living in syntopy.

Phenotypic and genetic divergence are shaped by the homogenizing effects of gene flow and the differentiating processes of genetic drift and local adaptation. Herein, we examined the mechanisms that underlie phenotypic (size and color) and genetic divergence in 35 populations (535 individuals) of the poison frog Epipedobates anthonyi along four elevational gradients (0–1800 m asl) in the Ecuadorian Andes. We found phenotypic divergence in size and color despite relatively low genetic divergence at neutral microsatellite loci. Genetic and phenotypic divergence were both explained by landscape resistance between sites (isolation-by-resistance, IBR), likely due to a cold and dry mountain ridge between the northern and southern elevational transects that limits dispersal and separates two color morphs. Moreover, environmental differences among sites also explained genetic and phenotypic divergence, suggesting isolation-by-environment (IBE). When northern and southern transects were analyzed separately, genetic divergence was predicted either by distance (isolation-by-distance, IBD; northern) or environmental resistance between sites (IBR; southern). In contrast, phenotypic divergence was primarily explained by environmental differences among sites, supporting the IBE hypothesis. These results indicate that although distance and geographic barriers are important drivers of population divergence, environmental variation has a two-fold effect on population divergence. On the one hand, landscape resistance between sites reduces gene flow (IBR), while on the other hand, environmental differences among sites exert divergent selective pressures on phenotypic traits (IBE). Our work highlights the importance of studying both genetic and phenotypic divergence to better understand the processes of population divergence and speciation along ecological gradients.

The efficacy of communication relies on detection of species-specific signals against the background noise. Features affecting signal detection are thus expected to evolve under selective pressures represented by masking noise. Spectral partitioning between the auditory signals of co-occurring species has been interpreted as the outcome of the selective effects of masking interference. However, masking interference depends not only on signal's frequency but on receiver's range of frequency sensitivity; moreover, selection on signal frequency can be confounded by selection on body size, because these traits are often correlated. To know whether geographic variation in communication traits agrees with predictions about masking interference effects, we tested the hypothesis that variation in the male-male communication system of the Amazonian frog, Allobates femoralis, is correlated with the occurrence of a single species calling within an overlapping frequency range, Epipedobates trivittatus. We studied frogs at eight sites, four where both species co-occur and four where A. femoralis occurs but E. trivittatus does not. To study the sender component of the communication system of A. femoralis and to describe the use of the spectral range, we analyzed the signal's spectral features of all coactive species at each site. To study the receiver component, we derived frequency-response curves from playback experiments conducted on territorial males of A. femoralis under natural conditions. Most geographic variation in studied traits was correlated with either call frequency or with response frequency range. The occurrence of E. trivittatus significantly predicted narrower and asymmetric frequency-response curves in A. femoralis, without concomitant differences in the call or in body size. The number of acoustically coactive species did not significantly predict variation in any of the studied traits. Our results strongly support that the receiver but not the sender component of the communication system changed due to masking interference by a single species.

Tropical anurans are among the most diverse and vulnerable organisms on Earth, yet the evolutionary mechanisms behind their diversity remain relatively unexplored. Epipedobates anthonyi is a poison frog that inhabits southern Ecuador and northern Peru along a broad elevational range (0–1800 m). Throughout its range, this species exhibits variation in phenotypic traits, such as color, advertisement calls, and alkaloid composition. The aim of this study is to isolate and characterize microsatellite loci to investigate patterns of genetic variation within the species. Using a next-generation sequencing approach to screen an enriched genomic library, we report twelve polymorphic microsatellite loci. The number of alleles per locus ranged from 7 to 15 per population. For the two populations tested, mean observed heterozygosity was 0.69 and 0.79, and mean expected heterozigosity was 0.84 and 0.85 respectively. Only locus EAN002 showed significant departure of HWE in both populations. None of the loci showed consistent null alleles in both populations. Also, no evidence of linkage disequilibrium was found across loci. In this paper, we report for the first time 12 microsatellite loci for E. anthonyi. These markers will be used to further elucidate evolutionary mechanisms underlying genetic and phenotypic variation across the species’ range.

The number of amphibian species described yearly shows no signs of slowing down, especially in tropical regions, implying that the biodiversity of amphibians remains woefully underestimated. A new species of poison frog is described from the Pacific lowlands of southwestern Colombia: Epipedobates currulao sp. nov. , named for the Pacific music and dance genre known as \"currulao\" or \"bambuco viejo\". This species inhabits lowland forests from 0–260 m a.s.l. This taxon differs from congeners by having a combination of bright yellow blotches in the dorsal anterior region of the thigh and upper arm, homogenous dark-brown dorsal coloration, and advertisement calls of long duration and many pulses. We also describe the courtship call of E. currulao sp. nov. , which is lower in frequency and shorter in duration than its advertisement call. Molecular phylogenetic analyses confirm the monophyly of the populations sampled and its position as the sister species of Epipedobates narinensis , which occurs in southwestern Colombia. Among species of Epipedobates , the new species has been previously confused with E. boulengeri , but the two species are allopatric and represent two divergent clades (1.77% divergent for 12S–16S and 5.39% for CYTB). These species can be distinguished by the presence of a bright yellow blotch on the dorsal anterior region of the thigh and on the upper arm of E. currulao sp. nov. , blotches that are either more white than yellow or absent in E. boulengeri . In addition, the advertisement calls are distinct, with E. currulao sp. nov. having a single but long call in each call series while E. boulengeri has 2–6 calls in a series with each call being much shorter in length. Epipedobates currulao sp. nov. is the most northern species of Epipedobates , which extends southwards along the western edge of the Andes. Known as the Chocó, this biogeographic region has been largely converted to agriculture in Ecuador and is experiencing widespread transformation in Colombia, which may endanger E. currulao sp. nov. and biodiversity in the region. A Spanish translation of the main text is available in Suppl. material 8.

Cardiotonic steroids (CTS) are a group of compounds known to be toxic due to their ability to inhibit the Na+/K+-ATPase (NKA), which is essential to maintain the balance of ions in animal cells. An evolutionary strategy of molecular adaptation to avoid self-intoxication acquired by CTS defended organisms and their predators is the structural modification of their NKA where specific amino acid substitutions confer resistant phenotypes. Several lineages of poison dart frogs (Dendrobatidae) are well known to sequester a wide variety of lipophilic alkaloids from their arthropod diet, however there is no evidence of CTS-sequestration or dietary exposure. Interestingly this study identified the presence of α-NKA isoforms (α1 and α2) with amino acid substitutions indicative of CTS-resistant phenotypes in skeletal muscle transcriptomes obtained from six species of dendrobatids: Phyllobates aurotaenia, Oophaga anchicayensis, Epipedobates boulengeri, Andinobates bombetes, Andinobates minutus, and Leucostethus brachistriatus, collected in the Valle del Cauca (Colombia). P. aurotaenia, A. minutus, and E. boulengeri presented two variants for α1-NKA, with one of them having these substitutions. In contrast, O. anchicayensis and A. bombetes have only one α1-NKA isoform with an amino acid sequence indicative of CTS susceptibility and an α2-NKA with one substitution that could confer a reduced affinity for CTS. The α1 and α2 isoforms of L. brachistriatus do not contain substitutions imparting CTS resistance. Our findings indicate that poison dart frogs express α-NKA isoforms with different affinities for CTS and the pattern of this expression might be influenced by factors related to evolutionary, physiological, ecological, and geographical burdens.

Assessments of extinction risk are required to inform conservation action, but the usefulness of assessments is undermined if they are not current. Ameerega planipaleae, a poison frog endemic to the cloud forests of central Peru, was last assessed in 2004. We therefore sought to provide updated data to inform the reassessment of this species. Based on our findings, we recommend that this frog remain categorized as Critically Endangered, but under modified criteria, and that conservation actions are taken to reduce the pressures of local threats, especially the overuse of agrochemicals.

Animal acoustic signals play seminal roles in mate attraction and regulation of male spacing, maintenance of pairbonds, localization of hosts by parasites, and feeding behavior. Among vertebrate signals, it is becoming clear that no single stereotyped signal feature reliably elicits species-specific behavior, but rather, that a suite of characters is involved. Within the largely nocturnal clade of anuran amphibians, the dart-poison frog, Epipedobates femoralis, is a diurnal species that physically and vigorously defends its calling territory against conspecific intruders. Here we report that physical attacks by a territorial male are provoked only in response to dynamic bimodal stimuli in which the acoustic playback of vocalizations is coupled with vocal sac pulsations, but not by either unimodal cues presented in isolation or static bimodal stimuli. These results suggest that integration of dynamic bimodal cues is necessary to elicit aggression in this species.