Independent evolutionary deterioration of the oxygen-transport system in Asian noodlefishes and Antarctic icefishes

Determination of evolutionary mechanisms underlying innovative traits is crucial for understanding the vast diversity of species and phenotypes. Given their respiratory physiologies, fishes are compelling subjects for evolutionary analysis of the hemoprotein-based oxygen-transport systems. Asian noodlefishes (Osmeriformes: Salangidae) and Antarctic icefishes (Notothenioidei: Channichthyidae) are examples of fish clades that generally do not express myoglobin or hemoglobin. To determine whether noodlefishes and icefishes share convergent or divergent patterns of hemoprotein loss, we sequenced the genomes of 11 species of the pedomorphic noodlefishes. We then compared noodlefish and icefish myoglobin genes and their α- and β-hemoglobin gene families. We document the complete loss of the myoglobin gene in Asian noodlefishes, a historical contingency that may have occurred by DNA transposon-mediated insertional mutagenesis prior to diversification of this clade. Previous results show independent losses of the myoglobin gene in 6 of 16 Antarctic icefishes. Neotenic development of noodlefishes prevented red blood cell production during the life histories of most species, and we show that genes encoding the α- and β-hemoglobins, haptoglobin, and hemogen deteriorated independently across noodlefish lineages. Icefishes, conversely, lost their hemoglobin genes as one or a few events, probably via transposon mutagenesis as we propose for noodlefish myoglobin genes. Genes involved in angiogenesis and heart development were under positive selection in noodlefishes and in icefishes, consistent with compensatory evolutionary adaptation of oxygen transport. We propose that deletion and disruption of hemoprotein genes in Asian noodlefishes and Antarctic icefishes occurred independently and that insertional mutagenesis was an important underlying molecular mechanism.