A pluralistic view on the evolutionary forces shaping genome size diversity in sharks

Abstract

Abstract Among vertebrates, sharks exhibit both large and heterogeneous genome sizes ranging from 2.86 to 17.05 pg. Aiming for a better understanding of the patterns and causalities of shark genome size evolution, we applied phylogenetic comparative methods to published genome-size estimates for 66 species representing the main phylogenetic lineages, life-histories and ecological traits. The 6-fold range of genome size variation was strongly traceable throughout the phylogeny, with a major expansion preceding shark diversification during the late Paleozoic and an ancestral state (6.37 pg) close to the present-day average (6.74 pg). Subsequent deviations from this average occurred at higher rates in squalomorph than in galeomorph sharks and were unconnected to evolutionary changes in the karyotype architecture, which were dominated by ascending disploidy events. Genome size was positively correlated with cell and nucleus sizes and negatively with metabolic rate. The metabolic constraints on increasing genome size also manifested at higher phenotypic scales, with large genomes associated with slow lifestyles, boreal latitudes, and purely marine waters. Moreover, large genome sizes were also linked to non-placental reproductive modes, which may entail metabolically less demanding embryological developments. Contrary to ray-finned fishes, genome size was associated neither with the taxonomic diversity of affected clades nor low genetic diversity.