The State of Squamate Genomics: Past, Present, and Future of Genome Research in the Most Speciose Terrestrial Vertebrate Order

Abstract

Squamates include more than 11,000 extant species of lizards, snakes, and amphisbaenians, and display a dazzling diversity of phenotypes across their over 200-million-year evolutionary history on Earth. Here, we introduce and define squamates (Order Squamata) and review the history and promise of genomic investigations into the patterns and processes governing squamate evolution, given recent technological advances in DNA sequencing, genome assembly, and evolutionary analysis. We survey the most recently available whole genome assemblies for squamates, including the taxonomic distribution of available squamate genomes, and assess their quality metrics and usefulness for research. We then focus on disagreements in squamate phylogenetic inference, how methods of high-throughput phylogenomics affect these inferences, and demonstrate the promise of whole genomes to settle or sustain persistent phylogenetic arguments for squamates. We review the role transposable elements play in vertebrate evolution, methods of transposable element annotation and analysis, and further demonstrate that through the understanding of the diversity, abundance, and activity of transposable elements in squamate genomes, squamates can be an ideal model for the evolution of genome size and structure in vertebrates. We discuss how squamate genomes can contribute to other areas of biological research such as venom systems, studies of phenotypic evolution, and sex determination. Because they represent more than 30% of the living species of amniote, squamates deserve a genome consortium on par with recent efforts for other amniotes (i.e., mammals and birds) that aim to sequence most of the extant families in a clade.

Differential Conservation and Loss of CR1 Retrotransposons in Squamates Reveals Lineage-Specific Genome Dynamics across Reptiles

“…We suggest that future studies consider the tradeoffs inherent to achieving a balance between data quantity for statistical power and data quality for reproducibility. In particular, the greater use of long-read sequencing technologies will improve TE annotation going forward (Gable et al 2023; Sproul et al 2023).…”

“…Comparative research in birds and mammals support an “accordion” model whereby DNA loss counteracts TE expansion (via transposition) and results in stable genome sizes over evolutionary timescales. Across squamates, genome size is tightly constrained (Pasquesi et al 2018; Armstrong et al 2020; Gable et al 2023), showing little variation across large phylogenetic distances. Our results suggest that while CR1 has been highly active over squamate evolutionary history, there is also evidence for the loss of CR1 subfamilies in the genomes of some squamate lineages, supporting an accordion model for squamates.…”

“…First described from the chicken genome ( Gallus gallus; Stumph et al 1984; International Chicken Genome Sequencing Consortium 2004), CR1 elements are similar to other vertebrate non-LTR retrotransposon families, such as L1 and L2, and are equipped with the machinery to “copy and paste” themselves into new genomic locations by retrotransposition using their own encoded proteins, including a reverse transcriptase (Ichiyanagi and Okada 2008). While CR1 is found only scarcely across mammalian genomes, which are instead dominated by L1 retrotransposons and non-autonomous retrotransposons (i.e., SINEs) (Chalopin et al 2015), CR1 is the dominant repetitive element in the genomes of birds and reptiles (i.e., sauropsids), comprising ∼4% of most avian genomes and up to 18% of some reptile genomes (Shedlock 2006; Shaffer et al 2013; Green et al 2014; Chalopin et al 2015; Pasquesi et al 2018; Gable et al 2023).…”

“…This suggests that the most ancient CR1 subfamilies otherwise shared across most amniotes have been lost in squamate genomes, as they have in birds. However, a lack of genome assemblies from representatives of many squamate lineages have only been made available very recently (Gable et al 2023; Pinto et al 2023; Card et al 2023), limiting our ability to accurately model ancestral states in reptile genome evolution (Shedlock 2006).…”

Karyotype Diversification and Chromosome Rearrangements in Squamate Reptiles

“…Lizards and snakes are characterized by a continuously updated taxonomy and complex phylogenetic relationships and by a high number of newly described species in the last few years (>500 between 2020 and 2023) [ 6 , 7 ]. Given their high biological and taxonomic diversity, squamates represent particularly promising model organisms in different fields of study such as evolutionary biology and genetics, evo-devo, historical biogeography, and conservation and invasion biology (e.g., [ 8 , 9 , 10 , 11 ]).…”