Anatomy and evolution of bioluminescent organs in the slimeheads (Teleostei: Trachichthyidae)

Bacterial bioluminescent organs in fishes have a diverse range of tissues of origin, patterns of compartmentalization, and associated light-conducting structures. The morphology of the perianal, bacterial bioluminescent organ of Aulotrachichthys prosthemius was described previously, but the light organ in other species of slimeheads, family Trachichthyidae, is poorly known. Here, we describe the anatomy of the bioluminescent organs in trachichthyids and places the evolution of this light-producing system in the context of a new phylogeny of the Trachichthyoidei to test the hypothesis that bioluminescence evolved twice in the suborder and that the light-producing component derives from the perianal ectoderm. We use gross and histological examination to provide the first description of the bioluminescent organ of Paratrachichthys and four additional species of Aulotrachichthys. Observations also strongly suggest the presence of a perianal bioluminescent organ in Sorosichthys ananasa. The updated phylogeny of the Trachichthyoidei is the first to combine morphological and DNA-sequence (11-gene fragments) evidence, and supports a monophyletic Trachichthyidae with component subfamilies Hoplostethinae and Trachichthyinae, supporting continued recognition of the family Anoplogastridae. All bioluminescent trachichthyoids share a similar bioluminescent-organ structure with elongate chambers filled with bacteria and connected to collecting ducts that, in turn, connect to superficial ducts that lead to and have lining epithelia continuous with the epidermis. In the context of the phylogeny, the bioluminescent organ of trachichthyids is inferred to have evolved as an elaboration of the proctodeum in the ancestor of Aulotrachichthys, Paratrachichthys, and Sorosichthys independently from the structurally similar cephalic bioluminescent organs in Anomalopidae and Monocentridae.