Phylogeography of the Central American lancehead Bothrops asper (SERPENTES: VIPERIDAE)

Abstract

The uplift and final connection of the Central American land bridge is considered the major event that allowed biotic exchange between vertebrate lineages of northern and southern origin in the New World. However, given the complex tectonics that shaped Middle America, there is still substantial controversy over details of this geographical reconnection, and its role in determining biogeographic patterns in the region. Here, we examine the phylogeography of Bothrops asper, a widely distributed pitviper in Middle America and northwestern South America, in an attempt to evaluate how the final Isthmian uplift and other biogeographical boundaries in the region influenced genealogical lineage divergence in this species. We examined sequence data from two mitochondrial genes (MT-CYB and MT-ND4) from 111 specimens of B. asper, representing 70 localities throughout the species’ distribution. We reconstructed phylogeographic patterns using maximum likelihood and Bayesian methods and estimated divergence time using the Bayesian relaxed clock method. Within the nominal species, an early split led to two divergent lineages of B. asper: one includes five phylogroups distributed in Caribbean Middle America and southwestern Ecuador, and the other comprises five other groups scattered in the Pacific slope of Isthmian Central America and northwestern South America. Our results provide evidence of a complex transition that involves at least two dispersal events into Middle America during the final closure of the Isthmus.

A complex biogeographic history of diversification in Neotropical lancehead pitvipers (Serpentes, Viperidae)

“…Currently, B. lanceolatus and B. caribbaeus inhabit the Martinique and Santa Lucía Islands, respectively, in the Lesser Antilles (Wüster, Thorpe, et al, ). Saldarriaga‐Córdoba, Parkinson, Daza, Wüster, and Sasa () consider an alternative hypothesis to explain the allopatric distribution of B. atrox group and B. asper lineages on each side of the Eastern Andes Cordillera, suggesting that the final uplift of this mountain range played a significant role in the cladogenesis of these lanceheads. They report that B. asper stock would diverge to the west of the Eastern Andes, possible within the foothills along the Pacific coast of northern South America and that the uplift of the Panamanian land bridge would have played a role in the diversification within asper lineages.…”

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

“…For example, the Neotropical rattlesnake ( Crotalus durissus complex) dispersed from Central America during the middle Pleistocene and subsequently diversified in open and dry habitats in South America east of the Andes (Wüster et al, ). In contrast, the ancestors of the B. asper species complex originated in north‐western South America approximately 3.3 Ma and then independently colonized Central America and dispersed south through the narrow strip of lowlands west of the Andes (Salazar‐Valenzuela, ; Saldarriaga‐Córdoba et al, ). The present‐day distribution of the group is mainly restricted to lowland tropical rainforests in these areas (Campbell & Lamar, ), but as with other vertebrates (Miller, Bermingham, Klicka, Escalante, & Winker, ) its southern limit occurs in north‐western Peru where highly arid conditions during the last 3 Ma may have restricted their dispersal further south (Hartley & Chong, ).…”

“…Individuals collected were considered to belong to a single population if they were found within a 5 km radius of a given locality. Based on Alencar et al, ; Fenwick Gutberlet Evans and Parkinson (), Parkinson, Campbell, and Chippindale (), Saldarriaga‐Córdoba et al (), and Wüster, Salomao, Quijada‐Mascareñas, Thorpe, and BBBSP. (), we used three B. atrox samples from a single population in Amazonian Brazil as an appropriate outgroup.…”

“…They are also among the most common pitvipers in Latin America and the leading cause of snakebite accidents in humans across their distribution (Otero‐Patiño, ; Warrell, ). Recent analyses based on mitochondrial DNA and genomic‐scale single‐nucleotide polymorphism (SNP) datasets have shown that this species complex comprises 7–10 lineages, with the deepest divergence between (a) a Nuclear Central American (region comprising Chiapas in Mexico, Guatemala, Belize, El Salvador, Honduras and northern Nicaragua) (Cano, Schuster, & Morrone, ) clade and (b) an Isthmian Central American and South American clade estimated to have occurred around 3.2 Ma (Salazar‐Valenzuela, ; Saldarriaga‐Córdoba, Parkinson, Daza, Wüster, & Sasa, ) (Figure b).…”

“…Only three of these lineages are distributed in Nuclear Central America, where B. asper populations have been observed from sea level to 1,200–1,300 m, while most of the other genetic groups are present in South America where populations can be found as high as 2,640 m in the Andes (Campbell & Lamar, ). This mountain range had attained its current elevations by the time these snakes colonized the northern Andes and lineages arose in isolated dry inter‐Andean valleys in the highlands of Colombia and Ecuador (Gutberlet & Harvey, ; Salazar‐Valenzuela, ; Saldarriaga‐Córdoba et al, ; Werman, ). As such, an evaluation of the recent evolutionary dynamics involved in the lowland and highland differentiations of this ecologically dissimilar group should add to the limited knowledge of how recent evolutionary diversification in vertebrates has occurred in this highly diverse region.…”