Genome Evolution and the Future of Phylogenomics of Non-Avian Reptiles

SIMPLE SUMMARY: As a group of organisms, non-avian reptiles, most of which are the ~11,000 species of lizards and snakes, are an extraordinarily diverse group, displaying a greater diversity of genetic, genomic, and phenotypic traits than mammals or birds. Yet the number of genomes available for non-avian reptiles lags behind that for other major vertebrate groups. Here we review the diversity of genome structures and reproductive and genetic traits of non-avian reptiles and discuss how this diversity can fuel the next generation of whole-genome phylogenomic analyses. Whereas most higher-level phylogenies of non-avian reptile groups have been driven by a group of markers known as ultraconserved elements (UCEs), many other types of markers, some with likely greater information content than UCEs, exist and are easily mined bioinformatically from whole-genomes. We review methods for bioinformatically harvesting diverse marker sets from whole genomes and urge the community of herpetologists to band together to begin collaboratively constructing a large-scale, whole-genome tree of life for reptiles, a process that has already begun for birds and mammals. Such a resource would provide a much-needed high-level view of the phylogenetic relationships and patterns of genome evolution in this most diverse clade of amniotes. ABSTRACT: Non-avian reptiles comprise a large proportion of amniote vertebrate diversity, with squamate reptiles—lizards and snakes—recently overtaking birds as the most species-rich tetrapod radiation. Despite displaying an extraordinary diversity of phenotypic and genomic traits, genomic resources in non-avian reptiles have accumulated more slowly than they have in mammals and birds, the remaining amniotes. Here we review the remarkable natural history of non-avian reptiles, with a focus on the physical traits, genomic characteristics, and sequence compositional patterns that comprise key axes of variation across amniotes. We argue that the high evolutionary diversity of non-avian reptiles can fuel a new generation of whole-genome phylogenomic analyses. A survey of phylogenetic investigations in non-avian reptiles shows that sequence capture-based approaches are the most commonly used, with studies of markers known as ultraconserved elements (UCEs) especially well represented. However, many other types of markers exist and are increasingly being mined from genome assemblies in silico, including some with greater information potential than UCEs for certain investigations. We discuss the importance of high-quality genomic resources and methods for bioinformatically extracting a range of marker sets from genome assemblies. Finally, we encourage herpetologists working in genomics, genetics, evolutionary biology, and other fields to work collectively towards building genomic resources for non-avian reptiles, especially squamates, that rival those already in place for mammals and birds. Overall, the development of this cross-amniote phylogenomic tree of life will contribute to illuminate interesting dimensions of biodiversity across non-avian reptiles and broader amniotes.