Salazar Valenzuela, David
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Salazar Valenzuela, David
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Quito
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davidsalazar@uti.edu.ec
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26644312900

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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

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Venom variation in Bothrops asper lineages from North-Western South America

2020 , Mora-Obando D. , Salazar Valenzuela, David , Pla D. , Lomonte B. , Guerrero-Vargas J.A. , Ayerbe S. , Gibbs H.L. , Calvete J.J.

Bothrops asper is a venomous pitviper that is widely distributed and of clinical importance in Mesoamerica and northern South America, where it is responsible for 50–80% of all envenomations by Viperidae species. Previous work suggests that B. asper has a complex phylogeographic structure, with the existence of multiple evolutionarily distinct lineages, particularly in the inter-Andean valleys of north South America. To explore the impact of the evolutionary history of B. asper on venom composition, we have investigated geographic variation in the venom proteome of this species from the populations from the Pacific side of Ecuador and south-western Colombia. Among the 21 classes of venom components identified, proteins from mainly four major toxin families, snake venom metalloproteases (PI- and PII-SVMP), phospholipases A2 (K49- and D49-PLA2s), serine proteinases (SVSP), and C-type lectins-like (CTL) proteins are major contributors to the geographic variability in venom. Principal component analyses demonstrate significant differences in venom composition between B. asper lineages previously identified through combination of molecular, morphological and geographical data, and provide additional insights into the selection pressures modulating venom phenotypes on a geographic scale. In particular, altitudinal zonation within the Andean mountain range stands out as a key ecological factor promoting diversification in venom. In addition, the pattern of distribution of PLA2 molecules among B. asper venoms complements phylogenetic analysis in the reconstruction of the dispersal events that account for the current biogeographic distribution of the present-day species' phylogroups. Ontogenic variation was also evident among venoms from some Ecuadorian lineages, although this age-related variation was less extreme than reported in B. asper venoms from Costa Rica. The results of our study demonstrate a significant impact of phylogenetic history on venom composition in a pitviper and show how analyses of this variation can illuminate the timing of the cladogenesis and ecological events that shaped the current distribution of B. asper lineages. Biological significance: Bothrops asper, called “the ultimate pitviper” due to its defensive behavior, large body size, and medical importance, represents a species complex that is widely distributed from southern México southwards across north-western South America to north-western Perú. This work reports the characterization of the venom proteomes of B. asper lineages from the Pacific sides of Ecuador and south-western Colombia. Multivariate analyses indicate that variability in venom composition among the B. asper lineages is driven by proteins from four major toxin families, presumably in response to selection pressures created by recent and historical ecological conditions created by geological and climatic events from the Pliocene-Pleistocene to the present along the Central and South American Continental Divide. The emerging biogeographic pattern of venom variation, interpreted in the context of the current phylogenetic hypotheses, support and complement previously proposed evolutionary Plio-Pleistocene dispersal events that shaped the present-day distribution range of B. asper lineages. In addition, our venomics data indicate the occurrence of genetic exchange between Colombian and Pacific Costa Rican populations, which may have occurred during the second wave of B. asper migration into Mesoamerica. Our work represents a foundation for a future broader sampling and more complete “-omics” analyses to deepen our understanding of the patterns and causes of venom variation in this medically important pitviper. © 2020 Elsevier B.V.

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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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Divergence of tropical pitvipers promoted by independent colonization events of dry montane Andean habitats

2019 , Salazar Valenzuela, David , Kuch U. , Torres-Carvajal O. , Valencia J.H. , Gibbs H.L.

Aim: A poorly explored feature of the origin and maintenance of Neotropical biodiversity is how the evolutionary dynamics of colonization and differentiation in relation to lowland and highland habitats has impacted lineage formation. Most speciation models for this region have focused on vicariant events, whereas the need to assess the influence of demographic processes has been recognized only recently. We evaluate if the origin of Andean montane lineages of terciopelo pitvipers is explained by either of two historical processes that represent distinct phylogeographic mechanisms: differentiation by isolation within the highlands or different dispersal events from the lowlands. Location: Western Ecuador. Taxon: Terciopelo pitvipers (Bothrops asper species complex). Methods: We use genomic data and genetic clustering analyses, evaluation of historical migration between genetic clusters and demographic model selection to investigate recent diversification events in South America using a vertebrate group rarely explored in phylogeographic studies: tropical Andean snakes. Specifically, the origin of two Ecuadorian montane lineages of terciopelo pitvipers was evaluated given ambiguous phylogenetic relationships with the presumably ancestral Pacific lowland lineage. Results: Discrepancies of evolutionary relationships previously obtained with tree-like methods are resolved through the use of modelling approaches. We found strong support for the independent origin of montane lineages based on topologies inferred by maximum-likelihood trees and modelling approaches that take into account possible gene flow. This suggests dispersal rather than in-situ differentiation as the most likely mechanism by which the montane linages originated. Main conclusions: Recent large-scale studies have found support for identifying dispersal events as important drivers of diversification in the Neotropical region. We contribute to these ideas by identifying a fine-scale case in a rarely studied group of animals -Andean snakes- in which river valleys acted as an entrance for the upward colonization of montane dry habitats and subsequent ecological diversification. © 2019 John Wiley & Sons Ltd

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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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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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Recent lineage diversification in a venomous snake through dispersal across the Amazon River

2018 , Gibbs H.L. , Sovic M. , Amazonas D. , Chalkidis H. , Salazar Valenzuela, David , Moura-Da-Silva A.M.

Identifying the evolutionary and ecological mechanisms that drive lineage diversification in the species-rich tropics is of broad interest to evolutionary biologists. Here, we use phylogeographical and demographic analyses of genomescale RADseq data to assess the impact of a large geographical feature, the Amazon River, on lineage formation in a venomous pitviper, Bothrops atrox. We compared genetic differentiation in samples from four sites near Santarem, Brazil, that spanned the Amazon and represented major habitat types. A species delimitation analysis identified each population as a distinct evolutionary lineage while a species tree analysis with populations as taxa revealed a phylogenetic tree consistent with dispersal across the Amazon from north to south. Phylogenetic analyses of mitochondrial DNA variation confirmed this pattern and suggest that all lineages originated during the mid- to late Pleistocene. Historical demographic analyses support a population model of lineage formation through isolation between lineages with low ongoing migration between large populations and reject a model of differentiation through isolation by distance alone. The results provide a rare example of a phylogeographical pattern demonstrating dispersal over evolutionary timescales across a large tropical river and suggest a role for the Amazon River as a driver of in situ divergence both by impeding (but not preventing) gene flow and through parapatric differentiation along an ecological gradient. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society.

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Harlequin frog rediscoveries provide insights into species persistence in the face of drastic amphibian declines

2022 , Jaynes, K.E. , Páez-Vacas, M.I. , Salazar Valenzuela, David , Guayasamin, J.M. , Terán-Valdez, A. , Siavichay, F.R. , Fitzpatrick, S.W.

Amphibians face global declines, and it remains unclear the extent to which species have responded, and through what mechanisms, to persist in the face of emerging diseases and climate change. In recent years, the rediscovery of species considered possibly extinct has sparked public and scientific attention. These are hopeful cases in an otherwise bleak story. Yet, we know little about the population status of these rediscovered species, or the biology underlying their persistence. Here, we highlight the iconic Harlequin frogs (Bufonidae: Atelopus) as a system that was devastated by declines but now encompasses between 18 and 32 rediscoveries (25–37 % of possible extinctions) in the last two decades. Geographic distributions of rediscoveries closely match regional described species abundance, and rediscoveries are documented at elevations from 100 m to >3500 m, with no significant differences between mean historical and contemporary elevations. We also provide genomic data on six decimated species, with historical sample comparisons for two of the species and find a pattern of decreasing genetic variation the longer a species had been missing. Further, we document marked decrease in heterozygosity in one species, but not the other, indicating potential idiosyncratic consequences of declines. Finally, we discuss research priorities to guide the potential transition from amphibian declines to recoveries and to maximize conservation efforts. © 2022 The Authors

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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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Total-evidence phylogeny and evolutionary morphology of New World pitvipers (Serpentes: Viperidae: Crotalinae)

2023 , Carrasco P.A. , Koch C. , Grazziotin F.G. , Venegas P.J. , Chaparro J.C. , Scrocchi G.J. , Salazar Valenzuela, David , Leynaud G.C. , Mattoni C.I.

Crotalines (pitvipers) in the Americas are distributed from southern Canada to southern Argentina, and are represented by 13 genera and 163 species that constitute a monophyletic group. Their phylogenetic relationships have been assessed mostly based on DNA sequences, while morphological data have scarcely been used for phylogenetic inquiry. We present a total-evidence phylogeny of New World pitvipers, the most taxon/character comprehensive phylogeny to date. Our analysis includes all genera, morphological data from external morphology, cranial osteology and hemipenial morphology, and DNA sequences from mitochondrial and nuclear genes. We performed analyses with parsimony as an optimality criterion, using different schemes for character weighting. We evaluated the contribution of the different sources of characters to the phylogeny through analyses of reduced datasets and calculation of weighted homoplasy and retention indexes. We performed a morphological character analysis to identify synapomorphies for the main clades. In terms of biogeography, our results support a single colonization event of the Americas by pitvipers, and a cladogenetic event into a Neotropical clade and a North American/Neotropical clade. The results also shed light on the previously unstable position of some taxa, although they could not sufficiently resolve the position of Bothrops lojanus, which may lead to the paraphyly of either Bothrops or Bothrocophias. The morphological character analyses demonstrated that an important phylogenetic signal is contained in characters related to head scalation, the jaws and the dorsum of the skull, and allowed us to detect morphological convergences in external morphology associated with arboreality. © 2023 Willi Hennig Society.

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