Biology subjects

Cannatella, D. C.

Publications and source records attributed to Cannatella, D. C..

7 recordsLinked to original sources

bioRxiv2026

From diet to defense: serpin duplication and gene-expression evolution as putative contributors to poison-frog alkaloid sequestration

Diverse organisms use toxins as antipredator defenses. Although many taxa synthesize their toxins, dietary toxin acquisition is less documented, particularly in vertebrates. In poison frogs (Dendrobatidae), efficient sequestration of dietary alkaloids evolved at least three times from ancestors that bore at most trace concentrations of skin alkaloids. Yet molecular mechanisms underlying poison-frog sequestration remain poorly understood. We used two approaches to address this. First, we performed a broad phylogenetic analysis of the serpinA gene family, which includes serpina1-like/alkaloid-binding globulin (ABG), the putative dendrobatid alkaloid transporter, and biliverdin-binding serpins (BBSs), which bind and spectrally tune biliverdin in blue-green arboreal frogs. Second, we used an evolutionarily narrower but discovery-oriented liver gene-expression analysis, contrasting seven populations from two sequestering Epipedobates species, the most recent origin of sequestration among dendrobatids (<15 mya), with two trace-accumulating lineages, Silverstoneia and Hyloxalus. Phylogenetic analyses revealed extensive diversification of ABGs and BBS-like genes in Dendrobatidae, forming two and five major clades, respectively. These expansions reveal broader ligand-binding serpin diversity than previously recognized and indicate that alkaloid sequestration may involve multiple ABG paralogs. Gene-expression analyses revealed 23 candidate genes associated with small-molecule transport, xenobiotic metabolism, and immune response, including serpina1-like, which was overexpressed in Epipedobates. A co-expression network analysis independently placed 20 of the 23 candidates into four key modules (enriched for differentially-expressed genes, containing [≥]1 candidate, and correlated with sequestration). Our findings point to ligand-binding-protein diversification and coordinated gene-expression changes as major contributors to the evolution of alkaloid defenses in poison frogs.

evolutionary biology↗

bioRxiv2025

Parallel Sensory Compensation following Independent Subterranean Colonization by Groundwater Salamanders (Eurycea )

Lineages that have invaded subterranean environments have repeatedly evolved remarkable adaptations to life in darkness. However, observational and experimental studies in additional natural systems are needed to further our understanding of repeated evolution and convergence. In Texas, a radiation of groundwater salamanders (genus Eurycea), with independent invasions of subterranean karstic environments, offers an opportunity to investigate phenotypic convergence, parallel evolution, and the enhancement and regression of sensory systems. Adaptations to a troglobitic life in this clade includes morphological, behavioral, and physiological changes within and among species. Intraspecific and interspecific variation in morphology to the selective pressures of life underground allows for detailed examination of physical, behavioral, and physiological changes associated with subterranean adaptation within a comparative phylogenetic framework. We find a tradeoff between two sensory systems repeated across multiple subterranean Eurycea lineages: the degeneration of the eye and the expansion of the mechanosensory lateral line. The increase in anterior neuromast organs in subterranean lineages was positively correlated with the expression of paired box protein Pax-6, a conserved transcription factor important for vertebrate neurogenesis. Our results show a decreasing trend of PAX-6 labeling in the neuromasts of adult surface salamanders (E. nana) relative to the maintained labeling in subterranean species (E. rathbuni). Our results suggest a tradeoff in resource allocation between the development of optic and anterior lateral line sensory systems in surface and subterranean salamander lineages and provide a starting point for future evolutionary developmental investigations examining the genetic underpinnings of adaptive, repeated evolution in a novel system. Significance StatementUnder-explored subterranean environments in Central Texas harbor a phenotypically and taxonomically diverse radiation of groundwater salamanders, which we used to test the molecular and developmental bases for adaptive evolution in extreme environments. Using an integrative approach, we quantify the divergence and convergence of two sensory modalities: vision loss and mechanoreception. The divergent developmental and phenotypic tradeoffs have evolved several times in parallel among populations and species in this group. Understanding the evolutionary developmental processes responsible for these changes will further our understanding of adaptive, repeated evolution in a natural system.

evolutionary biology↗

bioRxiv2024

Passive accumulation of alkaloids in putatively non-toxic frogs challenges paradigms of the origins of acquired chemical defenses

Understanding the origins of novel, complex phenotypes is a major goal in evolutionary biology. Poison frogs of the family Dendrobatidae have evolved the novel ability to acquire alkaloids from their diet for chemical defense at least three times. However, taxon sampling for alkaloids has been biased towards colorful species, without similar attention paid to inconspicuous ones that are often assumed to be undefended. As a result, our understanding of how chemical defense evolved in this group is incomplete. Here we provide new data showing that, in contrast to previous studies, species from each undefended poison frog clade have measurable yet low amounts of alkaloids. We confirm that undefended dendrobatids regularly consume mites and ants, which are known sources of alkaloids. Thus, our data suggest that diet is insufficient to explain the defended phenotype. Our data support the existence of a phenotypic intermediate between toxin consumption and sequestration -- passive accumulation -- that differs from sequestration in that it involves no derived forms of transport and storage mechanisms yet results in low levels of toxin accumulation. We discuss the concept of passive accumulation and its potential role in the origin of chemical defenses in poison frogs and other toxin-sequestering organisms. In light of ideas from pharmacokinetics we incorporate new and old data from poison frogs into an evolutionary model that could help explain the origins of acquired chemical defenses in animals and provide insight into the molecular processes that govern the fate of ingested toxins. ResumenComprender los origenes de fenotipos novedosos y complejos es un objetivo central en biologia evolutiva. Las ranas venenosas de la familia Dendrobatidae han desarrollado una novedosa habilidad para adquirir alcaloides de su dieta como defensas quimicas, al menos tres veces. Sin embargo, el muestreo de taxones en busca de alcaloides ha estado sesgado hacia las especies coloridas, sin prestar atencion similar a las poco conspicuas que a menudo se presume, no tienen defensas. Como resultado, nuestra comprension de como evolucionan las defensas quimicas en este grupo es incompleta. Aqui, proporcionamos nuevos datos que muestran que, en contraste con estudios anteriores, las especies de cada clado de ranas venenosas no defendidas tienen cantidades bajas pero cuantificables de alcaloides. Confirmamos que los dendrobatidos no defendidos consumen regularmente acaros y hormigas, que son fuentes conocidas de alcaloides. Por lo tanto, nuestros datos sugieren que la dieta es insuficiente para explicar el fenotipo defendido. Nuestros datos respaldan la existencia de un fenotipo intermedio entre consumo y secuestro de toxinas (acumulacion pasiva), que difiere del secuestro en que no implica formas derivadas de mecanismos de transporte y almacenamiento, pero da lugar a bajos niveles de acumulacion de toxinas. Discutimos el concepto de acumulacion pasiva y su potencial rol en el origen de defensas quimicas en ranas venenosas y otros organismos que secuestran toxinas. Considerando ideas de farmacocinetica, incorporamos datos nuevos y antiguos de ranas venenosas dentro de un modelo evolutivo que podria ayudar a explicar los origenes de defensas quimicas adquiridas en animales, y proporcionar una vision de los procesos moleculares que regulan el destino de las toxinas ingeridas.

evolutionary biology↗

bioRxiv2024

Honoring the Afro-Colombian musical culture with the naming of Epipedobates sp. nov. (Anura: Dendrobatidae), a frog from the Pacific rainforests

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. We describe a new species of poison frog from the Pacific lowlands of southwestern Colombia: Epipedobates currulao sp. nov., named for the Pacific music and dance genre known as bambuco viejo or currulao. 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, 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 we find that 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, blotches that are either more white than yellow or absent in E. boulengeri. In addition, the advertisement calls are distinct, with E. currulao 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 is the most northern species of Epipedobates, which extends southwards along the western edge of the Andes. Known as the Choco, this biogeographic region has been largely converted to agriculture in Ecuador and is experiencing widespread transformation in Colombia, which may endanger E. currulao and biodiversity in the region. A Spanish translation of the main text is available in the Supplementary Materials. ResumenEl numero de especies de anfibios descritas cada ano continua aumentando, especialmente en las regiones tropicales, lo que implica que la biodiversidad de anfibios sigue siendo subestimada. Describimos una nueva especie de rana venenosa de las tierras bajas del Pacifico del suroccidente de Colombia: Epipedobates currulao sp. nov., nombrada asi por el genero de musica y danza del Pacifico conocido como bambuco viejo o currulao. Las ranas de esta especie habitan en bosques de tierras bajas desde el nivel del mar hasta los 260 m. Este taxon se diferencia de sus congeneres por tener una combinacion de manchas amarillas brillantes en la region dorsal anterior del muslo y los brazos, una coloracion dorsal homogenea marron oscuro y cantos de advertencia mas largos y en consecuencia con mayor numero de pulsos. Tambien describimos la llamada de cortejo de E. currulao, con menor frecuencia pico y duracion que la llamada de advertencia. Los analisis filogeneticos confirman la monofilia de la especie y su posicion como hermana de Epipedobates narinensis, la cual se distribuye en el suroccidente de Colombia. Entre las especies de Epipedobates, la nueva especie ha sido previamente asignada a E. boulengeri, pero las dos especies son alopatricas y representan dos clados filogeneticamente divergentes (1.77% divergentes para 12S-16S y 5.39% para CYTB). Estas especies se pueden distinguir fenotipicamente por la presencia de una mancha amarilla brillante en la region dorsal anterior del muslo y en la parte superior del brazo en E. currulao, que son mas blancas que amarillas o estan ausentes en E. boulengeri. Ademas, los cantos de advertencia son distintos, E. currulao tiene una unica y larga llamada en una serie de llamadas, mientras que E. boulengeri tiene de 2 a 6 llamadas por serie, siendo cada llamada mucho mas corta. Epipedobates currulao es la especie distribuida mas al norte del genero Epipedobates, el cual se extiende hacia el sur a lo largo del flanco occidental de la cordillera de los Andes. Esta region conocida como el Choco biogeografico, ha sido fuertemente transformada por agricultura en Ecuador y esta experimentando una transformacion generalizada de sus bosques en Colombia, lo cual pone en peligro a E. currulao y toda su biodiversidad en un futuro cercano. Una traduccion al espanol del texto principal esta disponible en el material suplementario.

zoology↗

bioRxiv2023

Deep Divergences Among Cryptic Clades of Epipedobates Poison Frogs

Poison frogs (Dendrobatidae) are famous for their aposematic species, having a combination of diverse color patterns and defensive skin toxins, yet most species in this family are inconspicuously colored and considered non-aposematic. Epipedobates is among the youngest genus-level clades of Dendrobatidae that includes both aposematic and inconspicuous species. Using Sanger-sequenced mitochondrial and nuclear markers, we demonstrate deep genetic divergences among inconspicuous species of Epipedobates but relatively shallow genetic divergences among conspicuous species. Our phylogenetic analysis includes broad geographic sampling of the inconspicuous lineages typically identified as E. boulengeri and E. espinosai, which reveals two putative new species, one in west-central Colombia (E. sp. 1) and the other in north-central Ecuador (E. aff. espinosai). We conclude that E. darwinwallacei is a junior subjective synonym of E. espinosai. We also clarify the geographic distributions of inconspicuous Epipedobates species including the widespread E. boulengeri. We provide a qualitative assessment of the phenotypic diversity in each nominal species, with a focus on the color and pattern of inconspicuous species. We conclude that Epipedobates contains eight known valid species, six of which are inconspicuous. A relaxed molecular clock analysis suggests that the most recent common ancestor of Epipedobates is [~]11.1 million years old, which nearly doubles previous estimates. Last, genetic information points to a center of species diversity in the Choco at the southwestern border of Colombia with Ecuador. A Spanish translation this text is available in the supplementary materials on the publishers website (biorxiv does not allow posting in non-English languages).

evolutionary biology↗

bioRxiv2023

A potential cost of evolving epibatidine resistance in poison frogs

BackgroundSome poison arrow frogs sequester the toxin epibatidine as a defense against predators. We previously identified a single amino acid substitution (S108C) at a highly conserved site in a neuronal nicotinic acetylcholine receptor (nAChR) {beta}2 subunit that prevents epibatidine from binding to this receptor. When placed in a homologous mammalian nAChR this substitution minimized epibatidine binding but also perturbed acetylcholine binding, a clear cost. However, in the nAChRs of poison arrow frogs, this substitution appeared to have no detrimental effect on acetylcholine binding and, thus, appeared cost-free. ResultsThe introduction of S108C into the 4{beta}2 nAChRs of non-dendrobatid frogs also does not affect ACh sensitivity, when these receptors are expressed in Xenopus laevis oocytes. However, 4{beta}2 nAChRs with C108 had a decreased magnitude of neurotransmitter-induced currents in all species tested (Epipedobates anthonyi, non-dendrobatid frogs, as well as human), compared with 4{beta}2 nAChRs with the conserved S108. Immunolabeling of frog or human 4{beta}2 nAChRs in the plasma membrane using radiolabeled antibody against the {beta}2 nAChR subunit shows that C108 significantly decreased the number of cell-surface 4{beta}2 nAChRs, compared with S108. ConclusionsWhile S108C protects these species against sequestered epibatidine, it incurs a potential physiological cost of disrupted 4{beta}2 nAChR function. These results may explain the high conservation of a serine at this site in vertebrates, as well as provide an example of a tradeoff between beneficial and deleterious effects of an evolutionary change. They also provide important clues for future work on assembly and trafficking of this important neurotransmitter receptor.

evolutionary biology↗

bioRxiv2022

Diurnality shapes the visual opsin genes of colorful Neotropical frogs

Amphibians are ideal for studying visual system evolution because their biphasic (aquatic and terrestrial) life history and ecological diversity expose them to a broad range of visual conditions. Here we evaluate signatures of selection on visual opsin genes across Neotropical anurans and focus on three diurnal clades that are well-known for the concurrence of conspicuous colors and chemical defense (i.e., aposematism): poison frogs (Dendrobatidae), Harlequin toads (Bufonidae: Atelopus), and pumpkin toadlets (Brachycephalidae: Brachycephalus). We found evidence of positive selection on 44 amino acid sites in LWS, SWS1, SWS2, and RH1 opsin genes, of which one in LWS and two in RH1 have been previously identified as spectral tuning sites in other vertebrates. Given that anurans have mostly nocturnal habits, the patterns of selection revealed new sites that might be important in spectral tuning for frogs, potentially for adaptation to diurnal habits and for color-based intraspecific communication. Furthermore, we provide evidence that SWS2, normally expressed in rod cells in amphibians, has likely been lost in the ancestor of Dendrobatidae, suggesting that under low-light levels, dendrobatids have inferior wavelength discrimination compared to other frogs. This loss might follow the origin of diurnal activity in dendrobatids and could have implications for their chemical ecology, biodiversity, and behavior. Our analyses show that assessments of opsin diversification in understudied groups could expand our understanding of the role of sensory system evolution in ecological adaptation.

evolutionary biology↗