Comparative genomics of mobulid rays using a novel West Atlantic pygmy devil ray (Mobula hypostoma) reference genome

Abstract

Elasmobranchs are a subclass of cartilaginous fishes comprising around 1200 species of sharks, rays and skates. A combination of low-reproductive history traits and threats such as habitat destruction, overfishing and climate change, has led to a dramatic decline in elasmobranch population numbers. In recent years, elasmobranch conservation and stock management have increasingly relied on molecular data to understand speciation, habitat use and population dynamics; simultaneously, the past decade has seen an increased recognition of elasmobranchs as an important deep-branching clade in comparative studies aimed at understanding vertebrate evolution. Therefore, a growing body of high-quality, whole-genome sequences have been assembled for several elasmobranch species across most orders, including mobulid rays.

Mobulid rays, manta and devil ray species of genus Mobula, are highly derived batoid fishes with unique morphological features including cephalic lobes framing a forward-facing mouth; in contrast to ancestral ray and skate lineages, who are typically adapted to benthic environments, mobulids have evolved to expand into pelagic niches. Despite their endangered status, mobulid rays remain poorly studied and understood among cartilaginous fishes, including the genomic basis for their ecological adaptations and possible susceptibilities to environmental change. Therefore, the assembly of a novel chromosome-level, high-quality reference genome for the Atlantic pygmy devil ray, Mobula hypostoma, provides a unique opportunity to investigate mobulid evolutionary history and adaptation, and support future conservation studies.

Whole-genome alignment of M. hypostoma, with its sister species oceanic manta ray (M. birostris), Atlantic stingray (Hypanus sabinus) and two skate (Leucoraja erinacea and Amblyraja radiata) reference assemblies, was carried out using Cactus. De novo repeat libraries were constructed using RepeatMasker to characterise and compare the repeat landscape of each aligned species. Synteny analysis, homology relationships and structural rearrangements between these genomes were investigated to highlight mobulid-specific mutations. Functional annotation of mobulid – and M. hypostoma – specific genomic rearrangements was carried out to investigate their effects on genes and phenotype.

Results showed one-to one chromosome homology was mostly maintained between the two mobulid species, reflecting their recent divergence; in contrast, more substantial rearrangements were observed between mobulids and stingray, mostly chromosomal fusions. Repeats accounted for most of the genome content for all species (60-65%), with M. hypostoma possessing the highest genome content across all five batoids, and the highest percentage of DNA transposons and retroelements. Genomic regions lost in the mobulid ancestor directly impacted or were located near to many candidate genes associated with vertebrate craniofacial development, including alx3, fgf4, foxe1 among others. Further research will be needed to determine if these genomic changes were responsible.