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Resistance Is Not Futile: Widespread Convergent Evolution of Resistance to Alpha-Neurotoxic Snake Venoms in Caecilians (Amphibia: Gymnophiona)

2023 , Mancuso M. , Zaman S. , Maddock S.T. , Kamei R.G. , Salazar Valenzuela, David , Wilkinson M. , Roelants K. , Fry B.G.

Predatory innovations impose reciprocal selection pressures upon prey. The evolution of snake venom alpha-neurotoxins has triggered the corresponding evolution of resistance in the post-synaptic nicotinic acetylcholine receptors of prey in a complex chemical arms race. All other things being equal, animals like caecilians (an Order of legless amphibians) are quite vulnerable to predation by fossorial elapid snakes and their powerful alpha-neurotoxic venoms; thus, they are under strong selective pressure. Here, we sequenced the nicotinic acetylcholine receptor alpha-1 subunit of 37 caecilian species, representing all currently known families of caecilians from across the Americas, Africa, and Asia, including species endemic to the Seychelles. Three types of resistance were identified: (1) steric hindrance from N-glycosylated asparagines; (2) secondary structural changes due to the replacement of proline by another amino acid; and (3) electrostatic charge repulsion of the positively charged neurotoxins, through the introduction of a positively charged amino acid into the toxin-binding site. We demonstrated that resistance to alpha-neurotoxins convergently evolved at least fifteen times across the caecilian tree (three times in Africa, seven times in the Americas, and five times in Asia). Additionally, as several species were shown to possess multiple resistance modifications acting synergistically, caecilians must have undergone at least 20 separate events involving the origin of toxin resistance. On the other hand, resistance in non-caecilian amphibians was found to be limited to five origins. Together, the mutations underlying resistance in caecilians constitute a robust signature of positive selection which strongly correlates with elapid presence through both space (sympatry with caecilian-eating elapids) and time (Cenozoic radiation of elapids). Our study demonstrates the extent of convergent evolution that can be expected when a single widespread predatory adaptation triggers parallel evolutionary arms races at a global scale. © 2023 by the authors.

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Neotropics as a Cradle for Adaptive Radiations

2025 , Juan E. Guevara-Andino , Liliana M. Dávalos , Felipe Zapata , María José Endara , Darko D. Cotoras , Jaime Chaves , Santiago Claramunt , Julia López-Delgado , Angela M. Mendoza-Henao , Salazar Valenzuela, David , Gonzalo Rivas-Torres , Justin Yeager

Neotropical ecosystems are renowned for numerous examples of adaptive radiation in both plants and animals resulting in high levels of biodiversity and endemism. However, we still lack a comprehensive review of the abiotic and biotic factors that contribute to these adaptive radiations. To fill this gap, we delve into the geological history of the region, including the role of tectonic events such as the Andean uplift, the formation of the Isthmus of Panama, and the emergence of the Guiana and Brazilian Shields. We also explore the role of ecological opportunities created by the emergence of new habitats, as well as the role of key innovations, such as novel feeding strategies or reproductive mechanisms. We discuss different examples of adaptive radiation, including classic ones like Darwin's finches and Anolis lizards, and more recent ones like bromeliads and lupines. Finally, we propose new examples of adaptive radiations mediated by ecological interactions in their geological context. By doing so, we provide insights into the complex interplay of factors that contributed to the remarkable diversity of life in the Neotropics and highlight the importance of this region in understanding the origins of biodiversity.

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Evaluating the utility of camera traps in field studies of predation

2019 , Akcali C.K. , Pérez-Mendoza H.A. , Salazar Valenzuela, David , Kikuchi D.W. , Guayasamin, Juan M. , Pfennig D.W.

Artificial prey techniques-wherein synthetic replicas of real organisms are placed in natural habitats-are widely used to study predation in the field.We investigated the extent to which videography could provide additional information to such studies. As a part of studies on aposematism and mimicry of coral snakes (Micrurus) and their mimics, observational data from 109 artificial snake prey were collected from video-recording camera traps in three locations in the Americas (terra firme forest, Tiputini Biodiversity Station, Ecuador; premontane wet forest, Nahá Reserve, Mexico; longleaf pine forest, Southeastern Coastal Plain, North Carolina, USA). During 1,536 camera days, a total of 268 observations of 20 putative snake predator species were recorded in the vicinity of artificial prey. Predators were observed to detect artificial prey 52 times, but only 21 attacks were recorded. Mammals were the most commonly recorded group of predators near replicas (243) and were responsible for most detections (48) and attacks (20). There was no difference between avian or mammalian predators in their probability of detecting replicas nor in their probability of attacking replicas after detecting them. Bite and beak marks left on clay replicas registered a higher ratio of avian:mammalian attacks than videos registered. Approximately 61.5% of artificial prey monitored with cameras remained undetected by predators throughout the duration of the experiments. Observational data collected from videos could provide more robust inferences on the relative fitness of different prey phenotypes, predator behavior, and the relative contribution of different predator species to selection on prey. However, we estimate that the level of predator activity necessary for the benefit of additional information that videos provide to be worth their financial costs is achieved in fewer than 20% of published artificial prey studies. Although we suggest future predation studies employing artificial prey to consider using videography as a tool to inspire new, more focused inquiry, the investment in camera traps is unlikely to be worth the expense for most artificial prey studies until the cost:benefit ratio decreases. © 2019 PeerJ Inc. All rights reserved.

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Why Do Some Lineages Radiate While Others Do Not? Perspectives for Future Research on Adaptive Radiations

2025 , Rishi De-Kayne , Rowan Schley , Julia M.I. Barth , Luke C. Campillo , Catalina Chaparro-Pedraza , Jahnavi Joshi , Walter Salzburger , Bert Van Bocxlaer , Darko D. Cotoras , Carmelo Fruciano , Anthony J. Geneva , Rosemary Gillespie , Joseph Heras , Stephan Koblmüller , Blake Matthews , Renske E. Onstein , Ole Seehausen , Pooja Singh , Erik I. Svensson , Salazar Valenzuela, David , Maarten P.M. Vanhove , Guinevere O.U. Wogan , Ryo Yamaguchi , Anne D. Yoder , José Cerca

Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation. This record is sourced from MEDLINE/PubMed, a database of the U.S. National Library of Medicine

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Feeding ecology of the Terciopelo pit viper snake (Bothrops asper) in Ecuador

2023 , Loaiza-Lange A. , Székely D , Torres-Carvajal O. , Tinoco N. , Salazar Valenzuela, David , Székely P.

Thoroughly documenting prey items and diet composition is crucial for understanding a predator’s role in the ecosystem. In gape restricted predators, such as snakes, documenting and analyzing the type and size of the prey is important to interpret their ecological role. We describe the diet patterns of a species of venomous snake, the Terciopelo pit viper (Bothrops asper), from its Ecuadorian populations. Examining the gastrointestinal contents of museum specimens collected over an extensive area of the Pacific lowlands of Ecuador, we encountered 69 identifiable prey items from four major taxonomic groups (amphibians, centipedes, mammals, and reptiles). We evaluated the observed composition of prey to check for differences between sexes and size-classes. To complement our observations of the Terciopelo species complex throughout their distribution, we carried out a systematic literature review. Our data show an ontogenetic shift in diet, with a transition from more diverse diet in juveniles towards a mammal-specialized diet in adults, and distinct proportion of prey taxa between the sexes in the juvenile size class. Copyright 2023 Loaiza-Lange et al.

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Path for recovery: an ecological overview of the Jambato Harlequin Toad (Bufonidae: Atelopus ignescens) in its last known locality, Angamarca Valley, Ecuador

2024 , Mateo A. Vega-Yánez , Amanda B. Quezada-Riera , Blanca Rios-Touma , María del Carmen Vizcaíno-Barba , William Millingalli , Orlando Ganzino , Luis A. Coloma , Elicio E. Tapia , Nadine Dupérré , Mónica Páez-Vacas , David Parra-Puente , Daniela Franco-Mena , Gabriela Gavilanes , Salazar Valenzuela, David , Carlos A. Valle , Juan M. Guayasamin

The Jambato Harlequin toad (Atelopus ignescens), a formerly abundant species in the Andes of Ecuador, faced a dramatic population decline in the 1980s, with its last recorded sighting in 1988. The species was considered Extinct by the IUCN until 2016, when a fortuitous discovery of one Jambato by a local boy reignited hope. In this study, we present findings from an investigation conducted in the Angamarca parish, focusing on distribution, abundance, habitat preferences, ecology, disease susceptibility, and dietary habits of the species. In one year we identified 71 individuals at different stages of development in various habitats, with a significant presence in agricultural mosaic areas and locations near water sources used for crop irrigation, demonstrating the persistence of the species in a complex landscape, with considerable human intervention. The dietary analysis based on fecal samples indicated a diverse prey selection, primarily comprising arthropods such as Acari, Coleoptera, and ants. Amphibian declines have been associated with diseases and climate change; notably, our study confirmed the presence of the pathogen Batrachochytrium dendrobatidis (Bd), but, surprisingly, none of the infected Jambatos displayed visible signs of illness. When analyzing climatic patterns, we found that there are climatic differences between historical localities and Angamarca; the temporal analysis also exposes a generalized warming trend. Finally, in collaboration with the local community, we developed a series of management recommendations for terrestrial and aquatic environments occupied by the Jambato.

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A mouth full of blood – autohaemorrhaging in three Ecuadorian snakes (Squamata: Colubridae & Tropidophiidae)

2023 , Rödel M.-O. , Loaiza-Lange A. , Penner J. , Neira-Salamea K.D. , Salazar Valenzuela, David

[No abstract available]

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A First Look at the Inhibitory Potential of Urospatha sagittifolia (Araceae) Ethanolic Extract for Bothrops atrox Snakebite Envenomation

2022 , Vera-Palacios, A.L. , Sacoto-Torres, J.D. , Hernández-Altamirano, J.A. , Moreno, A. , Peñuela-Mora, M.C. , Salazar Valenzuela, David , Mogollón, N.G.S. , Almeida, J.R.

Bothrops atrox snakebites are a relevant problem in the Amazon basin. In this biodiverse region, the ethnomedicinal approach plays an important role as an alternative to antivenom therapy. Urospatha sagittifolia (Araceae) is a plant used for this purpose; however, its neutralizing properties have not been scientifically accessed. To fill this gap, we investigated the ability of U. sagittifolia to modulate the catalytic activity of Bothrops atrox venom, and their toxic consequences, such as local damage and lethality. The venom profile of B. atrox was assessed by chromatography and electrophoresis. Inhibition of the three main enzymatic and medically important toxins from the venom was evaluated using synthetic substrates and quantified by chromogenic activity assays. Additionally, the neutralization of lethality, hemorrhage and edema were investigated by in vivo assays. The possible interactions between venom proteins and plant molecules were visualized by polyacrylamide gel electrophoresis. Finally, the phytochemical constituents present in the ethanolic extract were determined by qualitative and quantitative analyses. The ethanolic extract reduced the activity of the three main enzymes of venom target, achieving ranges from 19% to 81% of inhibition. Our in vivo venom neuralizations assays showed a significant inhibition of edema (38.72%) and hemorrhage (42.90%). Additionally, lethality was remarkably counteracted. The highest extract ratio evaluated had a 75% survival rate. Our data support the biomedical value of U. sagittifolia as a source of natural enzyme inhibitors able to neutralize catalytically active B. atrox venom toxins and their toxic effects. © 2022 by the authors.

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Systematics of south american snail-eating snakes (Serpentes, dipsadini), with the description of five new species from ecuador and peru

2018 , Arteaga A. , Salazar Valenzuela, David , Mebert K. , Peñafiel N. , Aguiar G. , Sánchez-Nivicela J.C. , Alexander Pyron R. , Colston T.J. , Cisneros-Heredia D.F. , Yánez-Muñoz M.H. , Venegas P.J. , Guayasamin, Juan M. , Torres-Carvajal O.

A molecular phylogeny of the Neotropical snail-eating snakes (tribe Dipsadini) is presented including 43 (24 for the first time) of the 77 species, sampled for both nuclear and mitochondrial genes. Morphological and phylogenetic support was found for four new species of Dipsas and one of Sibon, which are described here based on their unique combination of molecular, meristic, and color pattern characteristics. Sibynomorphus is designated as a junior subjective synonym of Dipsas. Dipsas latifrontalis and D. palmeri are resurrected from the synonymy of D. peruana. Dipsas latifasciata is transferred from the synonymy of D. peruana to the synonymy of D. palmeri. A new name, D. jamespetersi, is erected for the taxon currently known as Sibynomorphus petersi. Re-descriptions of D. latifrontalis and D. peruana are presented, as well as the first photographic voucher of an adult specimen of D. latifrontalis, along with photographs of all known Ecuadorian Dipsadini species. The first country record of D. variegata in Ecuador is provided and D. oligozonata removed from the list of Peruvian herpetofauna. With these changes, the number of Dipsadini reported in Ecuador increases to 22, 18 species of Dipsas and four of Sibon. © 2018, Pensoft Publishers. All rights reserved.

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Bothrops atrox from Ecuadorian Amazon: Initial analyses of venoms from individuals

2021 , Patiño R.S.P. , Salazar Valenzuela, David , Medina-Villamizar E. , Mendes B. , Proaño-Bolaños C. , da Silva S.L. , Almeida J.R.

Bothrops atrox is the most clinically relevant snake species within the Amazon region, which includes Ecuadorian territories. It comprises a large distribution, which could contribute to the genetic and venomic variation identified in the species. The high variability and protein isoform diversity of its venom are of medical interest, since it can influence the clinical manifestations caused by envenomation and its treatment. However, in Ecuador there is insufficient information on the diversity of venomic phenotypes, even of relevant species such as B. atrox. Here, we characterized the biochemical and toxicological profiles of the venom of six B. atrox individuals from the Ecuadorian Amazon. Differences in catalytic activities of toxins, elution profiles in liquid chromatography, electrophoretic patterns, and toxic effects among the analyzed samples were identified. Nonetheless, in the preclinical testing of antivenom, two samples from Mera (Pastaza) required a higher dose to achieve total neutralization of lethality and hemorrhage. Taken together, these data highlight the importance of analyzing individual venoms in studies focused on the outcomes of envenoming. © 2021 Elsevier Ltd