A lizard is never late: squamate genomics as a recent catalyst for understanding sex chromosome and microchromosome evolution

Abstract

In 2011, the first high-quality genome assembly of a squamate reptile (lizard or snake) was published for the green anole. Dozens of genome assemblies were subsequently published over the next decade, yet these assemblies were largely inadequate for answering fundamental questions regarding genome evolution in squamates due to their lack of contiguity or annotation. As the "genomics age" was beginning to hit its stride in many organismal study systems, progress in squamates was largely stagnant following the publication of the green anole genome. In fact, zero high-quality (chromosome-level) squamate genomes were published between the years 2012-2017. However, since 2018, an exponential increase in high-quality genome assemblies has materialized with 24 additional high-quality genomes published for species across the squamate tree of life. As the field of squamate genomics is rapidly evolving, we provide a systematic review from an evolutionary genomics perspective. We collated a near-complete list of publicly available squamate genome assemblies from more than half-a-dozen international and third-party repositories and systematically evaluated them with regard to their overall quality, phylogenetic breadth, and usefulness for continuing to provide accurate and efficient insights into genome evolution across squamate reptiles. This review both highlights and catalogs the currently available genomic resources in squamates and their ability to address broader questions in vertebrates, specifically sex chromosome and microchromosome evolution, while addressing why squamates may have received less historical focus and has caused their progress in genomics to lag behind peer taxa.

Figure 1:

Chronological breakdown of genome assemblies published per-year and proportion of the assemblies that are chromosome-level (top panel) or annotated (bottom panel). Importantly, not all chromosome-level genomes are annotated and most chromosome-level assemblies that improve a previously annotated assembly do not publish updated annotations.

Figure 2:

Breakdown of total number of published genome assemblies (bar graph) per phylogenetic group (family or superfamily) co-plotted with number of species in each clade (branch colors and parenthetical numbers). Phylogeny from TimeTree using a representative species from each clade (Kumar et al. 2017), species counts from the Reptile Database (Uetz et al. 2022), and plotted using phytools (Revell, 2012).

Figure 3:

Time-calibrated phylogeny of squamate reptiles pruned to include only species with high-quality genome assemblies (rooted with chicken, Gallus gallus). Branches leading to major phylogenetic groups labeled, those with multiple taxa are highlighted. Phylogeny obtained from TimeTree (Kumar et al. 2017) and plotted using GeneSpace (Lovell et al. 2022) and FigTree [v1.4.4]. It’s apparent that microchromosomes are homologous in squamates that possess them (Salvator, Naja, and Shinisaurus), while different linkage group fusions have led to their loss in taxa that lack them (Sphaerodactylus and Podarcis).

Figure 4:

HiC contact maps for representative reptile taxa demonstrating the presence of microchromosomes in (A) birds and (B) teiids, or absence of microchromosomes in (C) geckos and (D) lacertids. Microchromosomes denoted with black bars to the bottom and right of the respective contact map. Annotation of microchromosomal organization denoted via top-right bracket in (A) and (B).