Systematics and Comparative Biogeography of Vine Snakes (Genus: Ahaetulla, Family: Colubridae) and Pit vipers (Genus: Trimeresurus, Family: Viperidae) in Peninsular India

Abstract

The Indian subcontinent is a considered a mega biodiverse region with representative regions belonging to three of the 35 global biodiversity hotspots, including the Western Ghats in Peninsular India and the Eastern Himalaya. These areas are threatened with biodiversity decline due to habitat loss and other factors such as climate change. Many species and populations may be extirpated even before they have been discovered, as these areas have not been adequately surveyed, especially for lower vertebrates and invertebrates. The region has over 300 species of snakes, but they are poorly studied despite the fact that snakes play an important ecological role in ecosystems, human landscapes and in medical science. Therefore, my study focused on the distribution and diversification of select taxa belonging to different families of snakes in Peninsular India, with an emphasis on systematics and biogeography. The evolution and biogeography of various taxa in Peninsular India are of particular interest as this region, a Gondawanan fragment, is critical to our understanding of historical biogeography in the Oriental realm. Over the past decade, molecular tools have enabled testing of alternative historical scenarios of faunal exchange and consequent biogeographic patterns. The snakes of Peninsular India, despite their spectacular diversity, remain known poorly with regard to their biogeographic affinities. While most Indian snakes are considered to be Malayan relicts, this hypothesis remains unexplored. I therefore explored the systematics and biogeography of snakes in the region. In addition, I used a phylogeographic framework to understand the genetic structure of widely distributed taxa which may comprise multiple lineages. I explored historical patterns of dispersal and diversification within Peninsular India using two distantly related snakes with broad differences in ecology and biology; an arboreal, non-venomous genus, Ahaetulla (vine snakes), belonging to the family Colubridae, and the genus Trimeresurus (Asian pit vipers), a group of terrestrial and arboreal, venomous snakes belonging to the family Viperidae. My broad objectives were to elucidate the historical biogeography of both snake genera in Peninsular India, more specifically, the role of vicariance and dispersal at broad spatial and temporal scales on observed patterns of distribution and diversity. At a regional scale, I also tested for patterns of lineage diversification within the Western Ghats region. To achieve these objectives, I used an extensive taxon sampling of snakes from Peninsular India and adjoining Northeast India with a comprehensive coverage of habitats and environmental gradients. With this dataset, I first delimited species using a coalescent method and a multicriteria approach including genes, geography and morphology. Second, using mitochondrial and nuclear DNA, I reconstructed the phylogenies and obtained a dated tree. Third, I tested for congruence in patterns of diversification and dispersal using ancestral range reconstruction of geographical ranges and diversification analyses. My dissertation is organized into the following chapters. Chapter 1 In this section, I introduce the patterns of distribution of snakes in the context of the biogeography of the Indian subcontinent with special reference to disjunct distributions in the wet evergreen parts of the Western Ghats and Northeast India. I discuss various hypotheses proposed to explain these patterns of distribution and the biogeographic affinities of snakes in the region. Two main processes have been proposed, namely dispersal and vicariance. The dispersal model suggests that lineages colonized different parts of Peninsular India through one or more routes of dispersal which may have appeared or disappeared over a period of time due to expansion and contraction of humid forest cover. The routes of colonisation proposed are through the Vindhya-Satpura hill ranges (known as the Satpura hypothesis), Eastern Ghats route or other routes from the Malayan region to Peninsular India. An alternative model, namely vicariance, suggests that a widespread ancestor of a lineage diverged in response to successive subdivisions of its distribution range. In addition to these broad biogeographic patterns, the complexity of the environmental gradient and ecological selection pressure could drive morphological variation leading to diversification. I provide an overview of patterns of distributions of snakes in India and their morphological variation I relation to geography and genetic structure. Finally, based on the broad distribution and diversity of taxa, I justify the value of snakes as a model system to study evolution and biogeography. Chapter 2 Genus Ahaetulla (family Colubridae) is distributed widely in Asia with nine species, of which three are endemic to India and seven are widely distributed. Species diversity in the drier and arid parts of Peninsular India is low compared to wet and humid areas. This is an understudied snake group in India, which includes a number of ecomorphs and color variations. A better understanding of the taxonomy and systematics of the group is required for both future ecological studies as well as for conservation. In addition, complete taxon sampling is needed to resolve uncertainties regarding the phylogenetic positions of lineages within this clade, including that of endemic species. Therefore, in this chapter, I present the first species delimitation and molecular systematics of vine snakes, incorporating all the known species across the Oriental region. I carried out comparisons between sister lineages which were identified with confidence due to our systematic sampling approach. The analysis revealed many cryptic species in vine snakes, which were delimited using a combination of genetics (phylogeny, Bayesian clustering algorithms and genetic distance), morphology and geography. In addition, I discovered a deeply divergent lineage from the southern Western Ghats, which is sister to all remaining members of Ahaetulla, and described it as a new genus, Proahaetulla. Chapter 3 Asian pit vipers belonging to the genus Trimeresurus are amongst the most diverse groups of vipers, and are distributed throughout Asia. Their distribution pattern is broadly similar to the genus Ahaetulla in Peninsular India. Species richness is low in drier and arid lowland parts of Peninsular India compared to wet and humid areas. In addition to resolving the taxonomy and systematics of lineages in Peninsular India, delimitation of species boundaries in widely distributed species is necessary for conservation and management and for further studies. In earlier studies, members of this clade had been assigned to different species or even genera (i.e Peltopelor in Peninsular India; Popeia, Viridovipera, Cryptelytrops in Northeast India) based on morphological characters, which needed to be revalidated using molecular tools. A taxonomic revision of Trimeresurus lineages from India is necessary to delimit species and understand their phylogenetic relationships and systematic position, and to revalidate the taxonomic status of ecomorphs within widely distributed species. Therefore, I carried out a delimitation of species boundaries in the genus Trimeresurus in India using a multicriteria approach including genetics, geography and morphology. I resolved the systematics of the group and assigned all members of the clade to the genus Trimeresurus; other proposed genera are not valid. In addition, I delimited multiple cryptic species within this group in the Western Ghats clade.

Chapter 4 Multiple colonization events of different taxa into and out of Peninsular India, and lineage diversification associated with past geographic and climatic events is expected to have shaped species richness in these snake genera, a pattern observed in many other taxa as well. To evaluate the pattern of colonization and diversification, I used independent evolutionary lineages from Chapters 2 and 3 for further phylogenetic and biogeographic analysis. For this, I used five genes to obtain a species tree; chronograms were reconstructed with available fossil calibrations. The resulting chronograms were used to reconstruct the biogeographic histories of both groups using ancestral area reconstructions. The patterns of dispersal show signatures of congruence and contrast between the clades, with the Western Ghats acting as a major source for colonisation of ancestral lineages into the arid regions in Peninsular India and adjoining Sri Lanka as well as Southeast Asian regions. I tested for alternative models of diversification with an emphasis on the Western Ghats. Ahaetulla supports a model of constant rate of speciation over time while Trimeresurus showed support for diversity dependent decline. In contrast to earlier hypotheses, Peninsular India emerged as a centre of snake diversification and Western Ghats as a major centre of in-situ radiation for both genera. Chapter 5 In this concluding section, I summarize the major findings from Chapters 2, 3 & 4. Both snake genera, Ahaetulla and Trimeresurus, consist of a number of cryptic lineages in Peninsular India. In the case of Ahaetulla, I discovered a deeply divergent lineage, sister to Ahaetulla, and described it as a new genus, Proahaetulla. The Western Ghats was found to be a major source for colonisation of ancestral lineages into the arid regions in Peninsular India and adjoining Sri Lanka as well as Southeast Asian regions. The region acts as a major centre of snake lineage diversification and in-situ radiation in Peninsular India.