Tracing genome size dynamics in sharks and rays with inclusive sequence analysis by the Squalomix Consortium

Genomes have maintained relatively stable gene sets during evolution, whereas chromosome organization and genome size vary drastically, even among vertebrates. Changes in genome size are often attributed to variable amounts of repetitive sequences, including transposable elements. However, it remains poorly understood what allows such drastic changes and how they affect various components of the genome and their functions. Elasmobranchs, including sharks, rays, and skates, exhibit high among-species variation of genome size and high within-species variation of chromosome length, offering a unique study system. In this study, we present the first whole-genome sequences of the whitebelly skate with relatively small genome size among elasmobranchs (2.2 Gb) and the red stingray. These chromosome-scale assemblies enable the assessment of genomic compositions including centromeres and noncoding elements, which reveal notable profiles of tRNA loci and unbiased intragenomic distribution of transposons in elasmobranch genomes. Comparative analyses across these species reveal a shared genomic architecture characterized by correlations of intergenic and intronic sequence lengths with chromosome sizes, with repetitive element accumulation in elongated regions. To assess whether elements beyond repetitive elements scale with genome size, we analyze tandem gene duplications and find they also tend to increase with genome expansion. In the quest for tandem genes, we characterize the first batoid HoxC cluster supported by transcriptional evidence in the red stingray genome, which has undergone extensive repetitive element invasion to unexpectedly colocalize with the HoxB cluster on a sex chromosome. Our study demonstrates an inclusive analysis encompassing both coding and noncoding regions, adaptable to diverse vertebrate taxa and a basis for molecular-level understanding on phenotypic diversity of elasmobranchs.