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

Abstract

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.

Phylogenetic Classification of Living and Fossil Ray-Finned Fishes (Actinopterygii)

“…The monophyly of Trachichthyiformes is supported in morphological (Zehren 1979;Moore 1993b;Baldwin and Johnson 1995;Konishi and Okiyama 1997) and molecular phylogenetic studies (Miya et al 2003(Miya et al , 2005; T. Grande et al 2013;Near et al 2013;Davis et al 2016;Betancur-R et al 2017;Dornburg et al 2017;Malmstrøm et al 2017;Musilova et al 2019;Ghedotti et al 2021;Ghezelayagh et al 2022;Mu et al 2022). Phylogenetic relationships among lineages of Trachichthyiformes inferred from morphological and molecular data differ substantially.…”

A new luminous roughy fish from northeastern Taiwan, with comments on congeners in Taiwan (Trachichthyidae: Aulotrachichthys)

“…Although Aulotrachichthys was initially established as a subgenus of Paratrachichthys by Fowler (1938), Gomon & Kuiter (1987) elevated it to a valid genus due to the presence of striated areas, a character shared with Sorosicthys but not Paratrachichthys . A recent phylogenetic and anatomic study conducted by Ghedotti et al (2021) showed that although not well-supported, Aulotrachichthys formed a monophyletic clade and is a sister clade with Sorosichthys and together formed a sister clade of Paratrachichthys . Moreover, they found that the structure of the light organ is different between Aulotrachichthys and Paratrachichthys .…”

“…Aulotrachichthys is characterized by having a rather slender body, body height at dorsal-fin origin < 40% standard length; its anus situated between pelvic-fin bases, and with a perianal bacterial bioluminescent organ; its body with a pair of silvery striated areas (tissue) along ventral-lateral side (Fig. 1); cycloid scales present between lateral line and pectoral-fin base; three to eight dorsal-fin spines; and six pelvic-fin soft rays (Gomon & Kuiter 1987, Kotlyar 1996, Ghedotti et al 2021, Matsunuma et al 2023).…”

Hoplostethus roseus, a new roughy fish from the western Pacific based on morphology and DNA barcoding (family Trachichthyidae)

“…Moreover, recognized four subgenera of Hoplostethus, i.e., Aulohoplostethus, Hoplostethus, Leiogaster and Macrohoplostethus, by the body colour, numbers of vertebrates, pyloric caeca and pectoral-fin rays, and size of abdominal scutes. Nonetheless, a recent phylogenetic study of Trachichthyoidei proposed by Ghedotti et al (2021) showed the polyphyly under Leiogaster and Hoplostethus. based his review and previous studies mostly on Russian material collected widely in the major oceans, including the southeastern Asian region around Japan and Taiwan, but did not report species specifically from Taiwanese waters.…”

“…Nonetheless, a recent phylogenetic study of Trachichthyoidei proposed by Ghedotti et al . (2021) showed the polyphyly under Leiogaster and Hoplostethus .…”