Exploring the phylogeny and depth evolution of cusk eels and their relatives (Ophidiiformes: Ophidioidei).

With 289 known species in 51 genera, the ophidiiform family Ophidiidae together with their relatives from the Carapidae (36 species in eight genera) of the same suborder Ophidioidei dominate the deep sea, but some occur also in shallow water habitats. Despite their high species diversity in the deep sea and wide bathymetric distributions, their phylogenetic relationships and evolution remain unexplored due in part to sampling difficulties. Thanks to the biodiversity exploratory program entitled "Tropical Deep-Sea Benthos" and joint efforts between Taiwan and French teams for sampling from different localities across the Indo-West Pacific over the last two decades, we are able to compile comprehensive datasets for investigations. In this study, 59 samples representing 36 of 59 known ophidioid genera are selected and used to construct a multi-gene dataset to infer the phylogenetic relationships of ophidioid fishes and their relatives. Our results reveal that the Ophidiidae forms a paraphyletic group with respect to the Carapidae. The four main clades of Ophidioidei resolved are the (1) clade comprising species from the subfamily Brotulinae; (2) clade that includes species in the genera Acanthonus and Xyelacyba; (3) clade grouping Hypopleuron caninum with species from the family Carapidae; and (4) clade containing the species in the subfamily Brotulotaenilinae, Neobythitinae (in part), and Ophidiinae. Accordingly, we suggest the following new revisions based on our results and proposed morphological diagnoses. The subfamily Brotulinae should be elevated to the family level. The genera Xyelacyba and probably Tauredophidium (unsampled in this study) should be included in the newly established family Acanthonidae with Acanthonus. The families Carapidae and Ophidiidae are re-defined. Our time-calibrated phylogenetic and ancestral depth reconstructions enable us to clarify the evolutionary history of ophidiiform fishes and infer past patterns of species distributions at different depths. While Ophidiiformes is inferred to have originated in shallow waters around 96.25 million years ago (Mya), the common ancestor to the Ophidioidei is inferred to have invaded the deep sea around 90.22 Mya, the dates coinciding with the global anoxic event of the OAE2. The observed bathymetric distribution patterns in Ophidioidei most likely point to the mesopelagic zone as the center of origin and diversification. This was followed by multiple events of depth transitions or range expansions towards either shallower waters or greater depth zones, which were likely triggered by past climate changes during the Paleogene-Neogene.