¿Are the venezuelan andes a species pump for atractus snakes (serpentes: dipsadidae)? contrasting the evolutionary and biogeographical history in three bioregions of Venezuela.
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Date
2025
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Universidad de Concepción
Abstract
La diversidad de especies puede variar considerablemente entre grupos taxonómicos y a lo largo del tiempo en un mismo linaje. Comprender estos procesos y mecanismos en relación con su diversificación en el Neotrópico constituye siempre un tema abierto en la biología evolutiva, sobre todo en las serpientes que han experimentado momentos explosivos de innovación trófica a lo largo de su historia evolutiva. Dentro de los dipsadinos, Atractus Wagler, 1828 representan una radiación de ~150 especies distribuidas por el Nuevo Mundo, desde el sur de Panamá hasta Argentina. El interés en este enigmático grupo de serpientes continúa creciendo debido, en parte, a su bioecología y distribución dominante en montañas, brinda una excelente oportunidad para investigar los patrones desde una perspectiva biogeográfica y evolutiva. Para examinar la diversificación y los patrones biogeográficos en este grupo de serpientes, reunimos un conjunto de datos multilocus ~3500 pb que abarca dos loci nucleares (NT 3 and RAG-1) y tres mitocondriales (16S, Cytb and ND4). Se implementaron análisis filogenéticos calibrados con fósiles y análisis de la tasa de diversificación subsiguiente mediante máxima verosimilitud e inferencia bayesiana para examinar su historia evolutiva y la dinámica temporal de la diversidad. Con base a esta idea, investigamos la dinámica de diversificación mediante la integración de múltiples enfoques filogenéticos y macroevolutivos (42 % de su diversidad). Los gráficos de linaje a través del tiempo (LTT) y las métricas de la tasa de diversificación (DR) indicaron una acumulación heterogénea de linajes, con cambios asociados a los eventos orogénicos andinos. Los modelos de diversificación dependiente de la densidad (DDD) sugirieron que la acumulación de linajes puede estar restringida por límites ecológicos, con evidencia que favorece los escenarios dependientes de la diversidad sobre los modelos de tasa constante. Los modelos dependientes del estado revelaron un papel de la geografía en la conformación de la diversificación: los análisis BiSSE respaldaron las diferencias en especiación y extinción vinculadas a las regiones andinas versus no andinas, mientras que los modelos ClaSSE destacaron la influencia de estados distribucionales complejos y procesos cladogenéticos. Complementariamente, los análisis BAMM detectaron heterogeneidad en la tasa de diversificación, identificando aceleraciones de la tasa en clados montanos. MEDUSA corroboró cambios significativos en la tasa a lo largo de la filogenia, en consonancia con una radiación en áreas topográficamente complejas. En conjunto, estos enfoques complementarios revelan que la diversificación de Atractus ha sido determinada por una combinación de oportunidades geográficas, limitaciones ecológicas y radiaciones impulsadas por las montañas (e.g, levantamiento de los Andes centrales y septentrionales). Hasta este momento, encontramos apoyo para el aumento de las tasas de especiación y extinción asociadas con los linajes Andinos vs. No Andinos, lo que respalda la hipótesis de que los Andes pudo haber funcionado como cuna o bomba de especies, debido a la heterogeneidad de paisajes y complejidad topográfica que favoreció la especiación alopátrica. Mientras, los análisis biogeográficos sugieren un origen en los Andes septentrionales hacia el Pacífico, alrededor de 22 Myr durante el Mioceno temprano, indicando una rápida radiación temprana seguida de una reciente disminución de la tasa de especiación. Finalmente, reevaluamos la sistemática del género en Venezuela por medio de una robusta delimitación de especies, con la ayuda de múltiples fuentes de evidencia, describiendo nuevas especies y evaluando su estatus de conservación. Este estudio proporciona un marco combinado de hipótesis evolutiva-biogeográfica, taxonómica y de conservación para entender la riqueza de estos dipsadinos y el papel del levantamiento andino en su diversificación y patrón biogeográfico.
Species diversity can vary considerably between taxonomic groups and over time within the same lineage. Understanding these processes and mechanisms in relation to their diversification in the Neotropics is always an open topic in evolutionary biology, especially in snakes that have experienced explosive moments of trophic innovation throughout their evolutionary history. Within the dipsadines, Atractus Wagler, 1828 represent a radiation of ~150 species distributed across the New World, from southern Panama to Argentina. Interest in this enigmatic group of snakes continues to grow, partly due to their bioecology and dominant distribution in mountains, providing an excellent opportunity to investigate patterns from a biogeographical and evolutionary perspective. To examine the diversification and biogeographic patterns in this group of snakes, we gathered a multilocus dataset of ~3500 bp encompassing two nuclear loci (NT-3 and RAG-1) and three mitochondrial loci (16S, Cytb, and ND4). Phylogenetic analyzes calibrated with fossils and subsequent diversification rate analyzes using maximum likelihood and Bayesian inference were implemented to examine their evolutionary history and the temporal dynamics of diversity. Based on this idea, we investigated the dynamics of diversification by integrating multiple phylogenetic and macroevolutionary approaches (42% of their diversity). The lineage-through-time (LTT) plots and diversification rate (DR) metrics indicated a heterogeneous accumulation of lineages, with changes associated with Andean orogenic events. Density-dependent diversification (DDD) models suggested that lineage accumulation may be restricted by ecological limits, with evidence favoring diversity-dependent scenarios over constant-rate models. State-dependent models revealed a role of geography in shaping diversification: BiSSE analyzes supported differences in speciation and extinction linked to Andean versus non-Andean regions, while ClaSSE models highlighted the influence of complex distributional states and cladogenetic processes. Complementarily, BAMM analyzes detected heterogeneity in the diversification rate, identifying rate accelerations in montane clades. MEDUSA corroborated significant changes in the rate throughout the phylogeny, in line with a radiation in topographically complex areas. Overall, these complementary approaches reveal that the diversification of Atractus has been determined by a combination of geographical opportunities, ecological limitations, and mountain-driven radiations (e.g., the uplift of the central and northern Andes). So far, we have found support for the increase in speciation and extinction rates associated with Andean vs. Non-Andean lineages, which supports the hypothesis that the Andes may have functioned as a cradle or species pump, due to the landscape heterogeneity and topographic complexity that favored allopatric speciation. Meanwhile, biogeographic analyzes suggest an origin in the northern Andes toward the Pacific, around 22 Myr during the early Miocene, indicating a rapid early radiation followed by a recent decline in the speciation rate. Finally, we reevaluated the systematics of the genus in Venezuela thru a robust species delimitation, with the help of multiple sources of evidence, describing new species and assessing their conservation status. This study provides a combined framework of evolutionary-biogeographic, taxonomic, and conservation hypotheses to understand the richness of these dipsadines and the role of the Andean uplift in their diversification and biogeographic pattern.
Species diversity can vary considerably between taxonomic groups and over time within the same lineage. Understanding these processes and mechanisms in relation to their diversification in the Neotropics is always an open topic in evolutionary biology, especially in snakes that have experienced explosive moments of trophic innovation throughout their evolutionary history. Within the dipsadines, Atractus Wagler, 1828 represent a radiation of ~150 species distributed across the New World, from southern Panama to Argentina. Interest in this enigmatic group of snakes continues to grow, partly due to their bioecology and dominant distribution in mountains, providing an excellent opportunity to investigate patterns from a biogeographical and evolutionary perspective. To examine the diversification and biogeographic patterns in this group of snakes, we gathered a multilocus dataset of ~3500 bp encompassing two nuclear loci (NT-3 and RAG-1) and three mitochondrial loci (16S, Cytb, and ND4). Phylogenetic analyzes calibrated with fossils and subsequent diversification rate analyzes using maximum likelihood and Bayesian inference were implemented to examine their evolutionary history and the temporal dynamics of diversity. Based on this idea, we investigated the dynamics of diversification by integrating multiple phylogenetic and macroevolutionary approaches (42% of their diversity). The lineage-through-time (LTT) plots and diversification rate (DR) metrics indicated a heterogeneous accumulation of lineages, with changes associated with Andean orogenic events. Density-dependent diversification (DDD) models suggested that lineage accumulation may be restricted by ecological limits, with evidence favoring diversity-dependent scenarios over constant-rate models. State-dependent models revealed a role of geography in shaping diversification: BiSSE analyzes supported differences in speciation and extinction linked to Andean versus non-Andean regions, while ClaSSE models highlighted the influence of complex distributional states and cladogenetic processes. Complementarily, BAMM analyzes detected heterogeneity in the diversification rate, identifying rate accelerations in montane clades. MEDUSA corroborated significant changes in the rate throughout the phylogeny, in line with a radiation in topographically complex areas. Overall, these complementary approaches reveal that the diversification of Atractus has been determined by a combination of geographical opportunities, ecological limitations, and mountain-driven radiations (e.g., the uplift of the central and northern Andes). So far, we have found support for the increase in speciation and extinction rates associated with Andean vs. Non-Andean lineages, which supports the hypothesis that the Andes may have functioned as a cradle or species pump, due to the landscape heterogeneity and topographic complexity that favored allopatric speciation. Meanwhile, biogeographic analyzes suggest an origin in the northern Andes toward the Pacific, around 22 Myr during the early Miocene, indicating a rapid early radiation followed by a recent decline in the speciation rate. Finally, we reevaluated the systematics of the genus in Venezuela thru a robust species delimitation, with the help of multiple sources of evidence, describing new species and assessing their conservation status. This study provides a combined framework of evolutionary-biogeographic, taxonomic, and conservation hypotheses to understand the richness of these dipsadines and the role of the Andean uplift in their diversification and biogeographic pattern.
Description
Tesis presentada para optar al grado de Doctor/a en Sistemática y Biodiversidad.
Keywords
Snakes, Biogeography, Endemic animals