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

Abstract

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.

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

“…To describe the diet of the B. asper complex in Ecuador ( Salazar-Valenzuela et al, 2019 ), we examined the gastro-intestinal tract (GIT) contents of 193 specimens (105 females and 88 males) from the collections of Museo de Zoología de la Pontificia Universidad Católica del Ecuador (QCAZ) and Museo de Zoología, Universidad Técnica Particular de Loja (MUTPL). Most of the examined specimens were fixed in 10% formalin and stored in 75% ethanol.…”

“…The Terciopelo pit vipers, Bothrops asper (Garman, 1883) species complex ( Salazar-Valenzuela, 2016 ; Saldarriaga-Córdoba et al, 2017 ; Salazar-Valenzuela et al, 2019 ; Mora-Obando et al, 2020 ), are highly adaptable venomous snakes distributed from eastern Mexico, throughout Central America, to Colombia and Venezuela (western and Caribbean), western lowlands of Ecuador, and down to the extreme northwestern Peru ( Solórzano & Cerdas, 1989 ; Campbell & Lamar, 2004 ; Cisneros-Heredia & Touzet, 2004 ). They occupy a wide range of ecosystems and have successfully adapted to modified habitats ( Campbell & Lamar, 2004 ; Sasa, Wasko & Lamar, 2009 ).…”

“…Kuch et al (2004) and Boada et al (2005) published the first accounts for populations in Ecuador, registering amphibians, birds, centipedes, insects, and mammals among prey items. Since these reports referred to specimens predominantly from the central-northern part of the country, a broader study that includes specimens from populations from the north and south of the country is needed, reflecting the lineage diversity shown by this species in Ecuador ( Salazar-Valenzuela et al, 2019 ).…”

What's in a mass?

“…Biogeographic studies support B. asper as the first species complex to split from the B. atrox clade in the Pliocene, ∼3.02-2.32 Mya, as the result of geological events, including the uplift of the Guanacaste, Central, and Talamanca mountain ranges in Mesoamerica, the late Miocene through the Pliocene; the closure of the Isthmus of Panamá; and the uplift of the Andes mountain range in South America. Habitat fragmentation promoted new ecological niche opportunities and led to allopatric speciation in these groups [36,37]. We have applied PLA 2 mass profiling to elucidate biogeographical patterns of the highly adaptable and widely distributed B. atrox and B. asper, which are considered the most dangerous snakes throughout much of their distribution range in the Amazon region (B. atrox) [31] and throughout Central America and west of the Andes in northern South America (B. asper) [32].…”

Viperidae snakebites in Ecuador: A review of epidemiological and ecological aspects

“…The species are separated from each other by the Andes and have no contact between them, except Bothrops lojanus, which can be found in these three Ecuadorian regions. It is possible that the movement of this species occurs through the Inter-Andean valley of Vilcabamba ( Torres-Carvajal et al, 2020 ; Salazar-Valenzuela et al, 2018 ; Valencia et al, 2016 ) ( Fig. 1 B and Table 1 ).…”