Phylogenomics and the origins of sharks

Abstract Genomes have the capacity to drastically modify hypotheses about the relationships of species. Despite the growing availability of non-model organism genome sequences, historically contentious portions of Tree of Life remain untested using genomic data. Here, we infer the phylogeny of sharks, skates, rays, and chimaeras using the genomes of 48 species, targeting different genomic marker types. Although phylogenetic relationships of chondrichthyans are relatively consistent across analyses, different molecular markers yield conflicting results about shark monophyly. Exons support the traditional view that sharks are monophyletic, whereas ultraconserved elements and legacy nuclear markers instead suggest that the frilled and cow sharks ( Hexanchiformes ), which retain the ancestral jaw structure of cartilaginous fishes, is the sister lineage of all other sharks and rays. The resolution of sharks as monophyletic or paraphyletic has little effect on inferences of the timescale of shark evolution or the origins of key traits, such as their ancestral ecology and genome size. We tie the diversification of living cartilaginous fishes to the transformation of marine ecosystems during the middle Mesozoic Era, confirming that living shark diversity is the product of rapid ancient diversification. Consequently, our results suggest that despite uncertainty around whether sharks are monophyletic, consensus can still be reached about major evolutionary events in this iconic vertebrate lineage. Significance Statement Living sharks, skates, rays, and chimaeras form one of the three principal groups of vertebrates. These iconic animals, which include over 1200 species, are key components of marine ecosystems and have helped us reconstruct the evolution of vertebrate genomes and phenotypes. However, much work on this group has assumed that sharks are a natural group. Here, for the first time, we leverage genome-scale data to test this hypothesis. Surprisingly, we show different genome regions reject or support hypothesis that sharks form a natural group to the exclusion of skates and rays. This throws an unexpected wrench into our understanding of the relationships of some of the oldest living vertebrate clades.