Paleoclimate determines diversification patterns in the fossorial snake family Uropeltidae Cuvier, 1829

https://doi.org/10.1016/j.ympev.2017.08.017Get rights and content

Highlights

  • First time-calibrated phylogeny of the family Uropeltidae representing all genera.

  • Asian anilioids experience a decrease in diversification rates at 11 Ma.

  • Diversification rate shift associated with forest contraction and fragmentation.

  • Significant correlation between diversification rate and paleotemperature.

  • Highlights the influence of environment on diversification of fossorial taxa.

Abstract

Understanding how and why diversification rates vary across evolutionary time is central to understanding how biodiversity is generated and maintained. Recent mathematical models that allow estimation of diversification rates across time from reconstructed phylogenies have enabled us to make inferences on how biodiversity copes with environmental change. Here, we explore patterns of temporal diversification in Uropeltidae, a diverse fossorial snake family. We generate a time-calibrated phylogenetic hypothesis for Uropeltidae and show a significant correlation between diversification rate and paleotemperature during the Cenozoic. We show that the temporal diversification pattern of this group is punctuated by one rate shift event with a decrease in diversification and turnover rate between ca. 11 Ma to present, but there is no strong support for mass extinction events. The analysis indicates higher turnover during periods of drastic climatic fluctuations and reduced diversification rates associated with contraction and fragmentation of forest habitats during the late Miocene. Our study highlights the influence of environmental fluctuations on diversification rates in fossorial taxa such as uropeltids, and raises conservation concerns related to present rate of climate change.

Introduction

Environmental factors play a key role in mediating diversification processes by driving microevolutionary change and shaping phenotypic evolution. Until recently, researchers had to rely on the paleontological record to understand how biotic and abiotic factors have influenced spatio-temporal diversification patterns (Barnosky, 2001, Benton, 2009, Vermeij, 1994, Vermeij, 1987). Fossil data are, however, incomplete, unevenly distributed in space and time and are not available for many taxa, limiting inferences on diversification processes to certain taxa (Benton et al., 2000, Valentine et al., 2006). Recently, the advent of mathematical models and analytical tools to estimate speciation and extinction rates from reconstructed phylogenies (Etienne et al., 2012, Morlon et al., 2011, Nee et al., 1994b, Rabosky, 2014, Rabosky, 2006, Stadler, 2011) have revolutionized the study of historical diversification patterns. These methods have allowed more precise inferences on the underlying evolutionary mechanisms and the factors that influence diversification rates.

Although fossil evidence suggests that the environment has had a strong influence on speciation and extinction dynamics (Ezard et al., 2011), the potential role of paleoclimatic fluctuations in influencing diversification rates in different taxa has not been explored in great detail. Climatic fluctuations can trigger shifts in species ranges (Barry et al., 1995, Thomas and Lennon, 1999) and thereby influence lineage diversification (Hou et al., 2011, Kolář et al., 2016, Pepper et al., 2011). Climate is also a driver of mass extinctions (Ivany et al., 2000, Lewis et al., 2008, Thomas, 1990), which not only prune branches off the tree of life (Green et al., 2011), but also influence lineages that survive by increasing ecological opportunity and thus enhancing diversification (Krug et al., 2009). A few empirical studies employing recently developed analytical tools to estimate diversification rates from molecular phylogenies suggest that paleoclimatic fluctuations have had a pronounced effect on diversification rates in several taxa (e.g. Birds – Claramunt and Cracraft, 2015, Jetz et al., 2012; Insects – Condamine et al., 2016; Spiny-rayed fish – Near et al., 2012; Amphibians – Roelants et al., 2007; Mammals – Stadler, 2011). Other studies have highlighted the pivotal role of mass extinctions in diversification rate variation (Krug et al., 2009, Longrich et al., 2012). Such studies, however, have been predominantly on aquatic and above ground terrestrial taxa. Fossorial taxa (i.e. those that are predominantly subterranean and burrow into the ground) have been largely ignored. The subterranean environment is structurally simple and thought to be relatively stable compared to above ground in terms of environmental fluctuations, and thus thought to persist relatively unchanged for millions of years (Gibert and Deharveng, 2002). However, how environmental factors influence temporal diversification in fossorial taxa and the macroevolutionary implications of fossoriality remain unexplored.

We here investigate temporal diversification patterns of the snake family Uropeltidae, a lineage of highly specialized fossorial snakes found predominantly in the moist forests in peninsular India and Sri Lanka. Phylogenetically, Uropeltidae is within the major clade Alethinophidia. Morphology and molecular based phylogenies of snakes have consistently placed Uropeltidae sister to Cylindrophidae (Hsiang et al., 2015, Pyron et al., 2013a, Slowinski and Lawson, 2002, Streicher and Wiens, 2016, Vidal and Hedges, 2002, Wiens et al., 2008), although a few studies place Anomochilidae as the sister group to Uropeltidae (Hsiang et al., 2015, Lee et al., 2007, Lee and Scanlon, 2002 (Hsiang et al., 2015, Lee et al., 2007, Lee and Scanlon, 2002). Together, the clade comprising Uropeltidae, Cylindrophidae and Anomochilidae is generally referred to as Asian anilioids.

Presently the family Uropeltidae is represented by ca. 55 species within nine genera – Melanophidium, Platyplectrurus, Teretrurus, Brachyophidium, Plectrurus, Pseudoplectrurus, Rhinophis, Pseudotyphlops and Uropeltis (Wallach et al., 2014) with some authors considering Pseudoplectrurus as a synonym of Rhinophis (Pyron et al., 2016). The relationships among these genera have remained largely unknown, and morphology and molecular based phylogenetic analyses have resulted in unresolved polytomies (Bossuyt et al., 2004, Olori and Bell, 2012, Rieppel and Zaher, 2002). Here we present a robust genus level phylogenetic hypothesis along with divergence time estimates. We show that the temporal diversification pattern was influenced by a single diversification rate shift correlated with paleoclimatic events during the Cenozoic.

Section snippets

Sampling

Sampling was carried out at multiple sites within the state of Kerala, Southern India. Collected samples were photographed, euthanized, fixed and preserved in ethanol, following which heart or liver tissues were collected and stored for DNA extraction. Additional tissue samples were obtained from ethanol preserved specimens deposited at the Zoological Survey of India – Western Ghat Regional Center (ZSI-WGRC).

DNA sequencing

Total genomic DNA was extracted using the standard Phenol-chloroform protocol (Bilton

Phylogenetic relationships

Maximum likelihood (RAxML) and Bayesian analyses (MrBayes and BEAST) consistently recovered four major clades – clade I: comprising the three species of Melanophidium; clade II: comprising Platyplectrurus, Teretrurus and Brachyophidium; clade III: comprising Pseudoplectrurus, Plectrurus, Indian and Sri Lankan Rhinophis, Pseudotyphlops and Sri Lankan Uropeltis; Clade IV: comprising the Indian Uropeltis. The topologies obtained from the Maximum likelihood and Bayesian inference on the combined

Phylogenetic relationships and biogeography

The two largest genera – Uropeltis and Rhinophis – were not recovered monophyletic. The Indian Uropeltis species formed a clade with high support. All three Sri Lankan Uropeltis formed a clade, which, grouped together with the Sri Lankan Rhinophis and the monotypic Sri Lankan endemic Pseudotyphlops. Pyron et al. (2016) in their recent phylogeny of Uropeltidae recovered the Sri Lankan uropeltids (Rhinophis, Uropeltis and Pseudotyphlops) as a single clade with the Indian Rhinophis travancoricus

Acknowledgments

We thank the Kerala Forest and Wildlife Department for providing collection permits under the order no. WL10-7451/2013 dated 06-04-2013 to the first author. We thank Umesh P. K., Anil Zachariah, Robin Abraham, David V. Raju, Ansil B. R., Dr. Jafer Palot, Kalesh S., Ram Prasad, Jobin Mathew, Sreejit Allipra, Tijo K. Joy, Arjun C. P., Johnson and Alex Johny for their assistance in field. We thank Ashok Kumar, Nithin Devakar, Anuraj, Varad Giri, Akshai Kandekar, Sreehari, Arun Zachariah, Snake

Funding

This work was supported by intra-mutual funds from IISER Thiruvananthapuram and the DST/INSPIRE Faculty Award from the Department of Science and Technology (Grant No. DST/INSPIRE/04/2013/000476) to UK.

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