The first report of luminescent liver tissue in fishes: Evolution and structure of bioluminescent organs in the deep-sea naked barracudinas (Aulopiformes: Lestidiidae)

Abstract

Bioluminescent organs that provide ventral camouflage are common among fishes in the meso-bathypelagic zones of the deep sea. However, the anatomical structures that have been modified to produce light vary substantially among different groups of fishes. Although the anatomical structure and evolutionary derivation of some of these organs have been well studied, the light organs of the naked barracudinas have received little scientific attention. This study describes the anatomy and evolution of bioluminescent organs in the Lestidiidae (naked barracudinas) in the context of a new phylogeny of barracudinas and closely related alepisauroid fishes. Gross and histological examination of bioluminescent organs or homologous structures from preserved museum specimens indicate that the ventral light organ is derived from hepatopancreatic tissue and that the antorbital spot in Lestrolepis is, in fact, a second dermal light organ. In the context of the phylogeny generated from DNA-sequence data from eight gene fragments (7 nuclear and 1 mitochondrial), a complex liver with a narrow ventral strand running along the ventral midline evolves first in the Lestidiidae. The ventral hepatopancreatic tissue later evolves into a ventral bioluminescent organ in the ancestor of Lestidium and Lestrolepis with the lineage leading to the genus Lestrolepis evolving a dermal antorbital bioluminescent organ, likely for light-intensity matching. This is the first described hepatopancreatic bioluminescent organ in fishes.

Phylogenetic classification of bony fishes

“…Lestidiidae is now recognized following MJ Ghedotti, RW Barton, AM Simons and MP Davis [217] and JS Nelson, T Grande and MVH Wilson [42].

Alepisauridae

Bathysauridae

Chlorophthalmidae (not monophyletic in Fig.

…”

Three new species of the barracudina genus Lestidium (Aulopiformes: Paralepididae) from the Indo-West Pacific

“…data), although some genetic studies separate it into two or more families (e.g. Ghedotti et al, 2015). They are found world-wide, mainly inhabiting deep pelagic waters of the outer continental shelf and slopes, and are important food for whales and swift predators (Rofen, 1966).…”

Morphology and evolution of bioluminescent organs in the glowbellies (Percomorpha: Acropomatidae) with comments on the taxonomy and phylogeny of Acropomatiformes

“…Bioluminescent organs in fishes are particularly diverse in their structure and anatomical derivation. Intrinsic bioluminescent organs that produce light directly may be evolutionarily and developmentally derived from integumentary, intestinal, muscle, or hepatopancreatic tissues (Ghedotti, Barton, Simons, & Davis, ; Johnston & Herring, ; Wassersug & Johnson, ), whereas bioluminescent organs that emit light via symbiotic bacteria have a more limited range of developmental origin, typically being restricted to structures contacting or closely associated with the external environment. Lineages of fishes that use their intrinsic or bacterially mediated bioluminescent organs for communication and sexual selection also have significantly increased rates of speciation relative to other lineages of bioluminescent fishes that primarily use light for camouflage (Davis et al, , ).…”