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.

The revised reference genome of the leopard gecko (Eublepharis macularius) provides insight into the considerations of genome phasing and assembly

“…Centromeres are a typical assembly breakpoint (Peona et al 2020) in genome assemblies but E. macularius has a karyotype consisting of 19 pairs of acrocentric chromosomes gradually decreasing in size (Gorman, 1973). Like other geckos, E. macularius chromosomes possess no sharp divide between macro- and microchromosomes (Figure 1; Pinto et al 2023). Thus, greater contiguity may be due, in part, to this chromosomal arrangement.…”

“…This is simultaneously the first phased chromosome-level assembly and the first long-read based genome assembly available for any species of gecko. Further, this assembly is one of the most contiguous squamate genomes available and has achieved the second highest BUSCO score of any squamate genome (Pinto et al 2023). The last hurdle for this assembly to overcome before this assembly can be considered a finished “telomere-to-telomere” assembly is placing the final 5.02Mb of unassembled sequence into the 19 primary scaffolds representing the 19 chromosomes of E. macularius .…”

“…Genomic data in squamate reptiles (lizards and snakes) has lagged behind other vertebrate model systems, such as birds and mammals, and high-quality reference genomes remain scarce (Bravo et al 2022; Hotaling et al 2021; Pinto et al 2023). Of the 23 previously published chromosome-scale squamate reference genomes, only 12 of the ~60 families are represented.…”

Incomplete dosage balance and dosage compensation in the ZZ/ZW Gila monster (Heloderma suspectum) revealed byde novogenome assembly

“…The final haploid genome assembly was 2.56Gb in total length, with a scaffold N50 of 7.86Mb and a contig N50 of 35.49Kb (Supplemental Tables S3 and S4). Interestingly, this genome assembly was the largest of any available available anguimorph genome, 70%, 25%, and 12% larger than Komodo dragon (V. komodoensis), Chinese crocodile lizard (S. crocodilurus), and beaded lizard (H. charlesbogerti) assemblies, respectively (Pinto et al, 2023). The assembled Gila monster genome was 97.2% completecalculated using kmers-with an average per-base error rate of 7.15316 x 10 -05 (i.e.…”

“…Perhaps most striking is the difference between male and female heterogametic systems: dosage balance and/or compensation are often observed in male heterogametic systems (XX/XY), while nearly all female heterogametic (ZZ/ZW) systems studied to date-other than Lepidoptera and a species of brine shrimp (Gu et al, 2019;Huylmans et al, 2017Huylmans et al, , 2019Walters et al, 2015)-exhibit a lack of dosage balance and incomplete dosage compensation (Gu & Walters, 2017). While putative mechanisms have been proposed to explain this difference (Mullon et al, 2015), dosage compensation has been studied in very few squamates and work in additional taxa is needed to better understand its evolution (Pinto et al, 2023).…”