Phylogenetics, systematics, and biogeography of Lygosoma group skinks (Squamata: Scincidae: Lygosominae) and Locomotor capacities of three lygosomine skinks from Thailand

Abstract

The lizard family Scincidae is the most species-rich family of squamate reptiles, comprising more than 1,600 species. Skinks are ecologically and morphologically diverse, occurring in tropical and temperate zones on all continents excluding Antarctica, as well as on many oceanic islands. Although skinks are a ubiquitous part of most of the world’s herpetofauna, we still lack a basic understanding of the evolutionary history and biodiversity of many clades within the family. Using molecular data, concatenated- and coalescent-based phylogenetic analyses, morphological datasets, and multivariate statistics, I reconstruct the evolutionary history of a clade of skinks called the Lygosoma group skinks, a group of elongate-bodied semifossorial species distributed across the Old World tropics in Africa, South Asia, Southeast Asia, and Sundaland. My dissertation focuses on the phylogenetics, systematics, taxonomy, species-level diversity, and biogeography of this group, and I address questions including: How are species related? What macroevolutionary factors have influenced species diversification across evolutionary time? And, how have historical processes shaped the modern biodiversity of Lygosoma group skinks? Additionally, I use high speed videos of locomotion and multivariate statistics to investigate the locomotor kinematics and performance of three species of co-distributed skinks in Thailand to address the following question: Does diversity in morphology result in diversity in locomotor performance and kinematics? The results of my dissertation provide insight into the evolutionary history and biodiversity of skinks in the Old World tropics. In my first chapter, I delve into the taxonomic history of Lygosoma group skinks and propose a new classification based on phylogeny generated with the most robust genetic and taxonomic sampling of the group to date. The genera Lepidothyris, Lygosoma and Mochlus comprise the writhing or supple skinks (Lygosoma s.l.), a group of semi-fossorial, elongate-bodied skinks distributed across the Old World Tropics. Due to their generalized morphology and lack of diagnostic characters, species- and clade-level relationships have long been debated. Recent molecular phylogenetic studies of the group have provided some clarification of species-level relationships, but a number of issues regarding higher level relationships among genera still remain. In this study, I present a phylogenetic estimate of relationships among species in Lygosoma, Mochlus and Lepidothyris generated by concatenated and species tree analyses of multilocus data using the most extensive taxonomic sampling of the group to date. I also use multivariate statistics to examine species and clade distributions in morphospace. The results reject the monophyly of Lygosoma s.l., Lygosoma s.s., and Mochlus, which highlights the instability of the current taxonomic classification of the radiation. Based on these findings, I revise the taxonomy of the writhing skinks to better reflect the evolutionary history of Lygosoma s.l. by restricting the genus Lygosoma to Southeast Asia, resurrecting the genus Riopa for a clade of Indian and Southeast Asian species, expanding the genus Mochlus to include all African species of writhing skinks, and describing a new genus in Southeast Asia. By providing a new classification for Lygosoma group skinks and the most robust species-level molecular phylogeny to date, this chapter establishes a new set of names for the group that are important in communicating about clades and species and facilitating future studies on evolution and diversification within this radiation of lizards. In my second chapter, I transition from a broad-scale study on biodiversity and systematics of Lygosoma group skinks and focus on fine-scale species-level diversity within the group. Specifically, I investigate the biodiversity of a species complex of skinks in the genus Riopa in Myanmar and show that the current species-level diversity of the group is highly underestimated. Recognizing species-level diversity is important for studying evolutionary patterns across biological disciplines and is critical for conservation efforts. However, challenges remain in delimiting species-level diversity, especially in cryptic radiations where species are genetically divergent but show little morphological differentiation. Using multilocus molecular data, phylogenetic analyses, species delimitation analyses, and morphological data, I examine lineage diversification in a cryptic radiation of Riopa skinks in Myanmar. Four species of Riopa skinks are currently recognized from Myanmar based on morphological traits, but the boundaries between three of these species, R. anguina, R. lineolata, and R. popae are not well-defined. I find high levels of genetic diversity within these three species, and analyses suggest that they may comprise as many as 12 independently evolving lineages, which highlights the extent to which species diversity in the region is underestimated. However, quantitative trait data suggest that these lineages have not differentiated morphologically, possibly indicating that this cryptic radiation represents a non-adaptive evolution, although additional data is needed to corroborate this. The results of this chapter provide essential data on the biodiversity of a clade of skinks in Myanmar, an understudied region, and are therefore important in conservation and management. Additionally, this study corroborates a previously recognized hypothesis that species-level diversification is high within the country’s Central Dry Zone. Finally, this study provides important information on the true species-level diversity of Myanmar Riopa, which is critical for future studies of diversification in Lygosoma group skinks. In my third chapter, I increase taxonomic and genetic sampling of my molecular dataset, including the additional lineages discovered in chapter two, to investigate the historical biogeography of Lygosoma group skinks across the Old World tropics. Through this research, I gain an understanding of how large-scale geological and climatic processes affected diversification of the group since the late Paleocene approximately 60 million years ago. Using Bayesian fossilized birth-death divergence dating for 40 ingroup lineages and species of Lygosoma group skinks, I reconstruct ancestral ranges and estimate shifts in evolutionary rates and species through time for all genera. Additionally, while logic suggests that geographic sampling has a large impact on biogeographic reconstructions of a clade, this result has never been demonstrated empirically. Therefore, I investigate the impact geographic sampling has on biogeographic analyses and the resulting ancestral range reconstructions by randomly sub-sampling the species in my analysis and rerunning biogeographic analyses to generate null distributions for the probabilities of ancestral ranges. The results of this study support early diversification of Lygosoma group skinks just over 50 mya from an ancestral range that included India, with subsequent dispersal throughout the Old World tropics. Diversification continued throughout the Eocene and Miocene and was not accompanied by shifts in evolutionary rates. Resampling analyses indicate that biogeographic reconstruction is strongly influenced by the geographic sampling of taxa. The biogeographic scenario I present in this chapter provides a testable hypothesis for future studies on paleontology, diversification, and trait evolution in Lygosoma group skinks. Additionally, the results emphasize the importance of taxonomic and geographic sampling in understanding the evolutionary history of clades, indicating that biodiversity surveys remain an essential part of phylogenetic and evolutionary research. In my fourth chapter, I take a different approach to understanding the biodiversity of skinks by investigating how differences in body morphology affect the performance and kinematics of three species of skinks in Thailand. The goal of this study is to if species with different morphologies maintain locomotor performance and the process by which this happens. Locomotion is an essential function in the life of vertebrates and higher locomotor performance is correlated with increased survival. Although studies over the past three decades have made substantial progress in understanding the locomotion and locomotor kinematics in squamate reptiles, we still lack an understanding of how locomotion occurs across the diversity of body forms in squamate reptiles. In this study, I investigate the locomotion and kinematics of three co-distributed skink species from Southeast Asia: Eutropis macularia, Sphenomorphus maculatus, and Subdoluseps bowringii-frontoparietale. I find that the more elongate species, Subdoluseps bowringii-frontoparietale, has greater axial bending, whereas Sphenomorphus maculatus, the species with the relatively longest hind limb length, has a higher maximum velocity. Additionally, the results show correlations between stride mechanics (stride duration, stride length, and duty factor) and maximum velocity across all three species and correlations between stride mechanics and morphology in Eutropis macularia and Sphenomorphus maculatus. Finally, statistical analyses suggest that the two robust-limbed species, Eutropis macularia and Sphenomorphus maculatus, have higher reliance on limbed propulsion during locomotion than Subdoluseps bowringii-frontoparietale. This study is the first to investigate locomotor performance and kinematics in these three species and corroborates most previous hypotheses of locomotion in squamate reptiles.