Cenozoic evolutionary history obscures the Mesozoic origins of acanthopterygian fishes.

Abstract

Sister lineage comparisons provide a valuable tool for understanding evolutionary origins of species-rich clades and the role of habitat transitions in lineage diversification. Percomorpha, comprising over 18,900 species, represents one of the most species-rich lineage of vertebrates. However, the phylogenetic resolution of its sister lineage remains unclear, obscuring whether contrasts in histories of diversification provide insights into the factors that gave rise to this clade's high diversity. Using 887 ultraconserved element loci and eight Sanger-sequenced nuclear genes, we resolve the phylogenetic relationships of the three closest relatives of Percomorpha-the roughies, flashlightfishes, porcupinefishes and fangtooths (Trachichthyiformes), the squirrelfishes and soldierfishes (Holocentridae), and the whalefishes, bigscales, and alfonsinos (Berycoidei)-and the placement of percomorphs among them. Contrary to expectations from the fossil record, we demonstrate that living lineages of Berycoidei, Holocentridae, and Trachichthyiformes all diversified after the Cretaceous-Paleogene mass extinction. Our findings show that multiple clades in Trachichthyiformes and Berycoidei independently colonized deep ocean habitats during the climatically unstable Eocene and Oligocene and shallow-water reefs during the extensive hotspot migration and faunal turnover of the Early Miocene. This coincided with the evolution of novel life history traits, including pelagic cnidarian-mimicking larvae and extreme sexual dimorphism in some deep-sea forms. Because of their recent invasions of these habitats, the closest relatives of Percomorpha are not ideal for understanding the origins of this exceptionally species-rich clade in the marine realm.