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

Abstract

Bioluminescent organs have evolved many times within teleost fishes and exhibit a wide range of complexity and anatomical derivation. Although some bioluminescent organs have been studied in detail, the morphology of the bacterial light organs in glowbellies (Acropoma) is largely unknown. This study describes the anatomy of the bioluminescent organs in Haneda's Glowbelly (Acropoma hanedai) and the Glowbelly (Acropoma japonicum) and places the evolution of this light‐producing system in the context of a new phylogeny of glowbellies and their relatives. Gross and histological examination of the bioluminescent organs indicate that they are derived from perianal ectodermal tissue, likely originating from the developmental proctodeum, contrary to at least one prior suggestion that the bioluminescent organ in Acropoma is of endodermal intestinal derivation. Additionally, anterior bioluminescent organ development in both species is associated with lateral spreading of the bacteria‐containing arms of the bioluminescent organ from an initial median structure. In the context of a 16‐gene molecular phylogeny, the bioluminescent organ in Acropoma is shown to have evolved within the Acropomatidae in the ancestor of Acropoma. Further, ancestral‐states reconstruction demonstrates that the bioluminescent organs in Acropoma evolved independently from the light organs in related howellid and epigonid taxa which have esophageal or intestinally derived bioluminescent organs. Across the acropomatiforms, our reconstructions indicate that bioluminescent organs evolved independently four or five times. Based on the inferred phylogeny of the order where Acropoma and Doederleinia were separated from other traditional acropomatids, the familial taxonomy of the Acropomatidae was modified such that the previously described Malakichthyidae and Synagropidae were recognized. We also morphologically diagnose and describe the family Lateolabracidae.

The Phylogeny of Carangiform Fishes: Morphological and Genomic Investigations of a New Fish Clade

“…OR centuries, studies on the evolution of fishes were based on surveys and analyses of anatomical characters. Comparisons among wet and dry skeletons (e.g., Olney et al, 1993;Holcroft and Wiley, 2015), and surveys of characters through different visualization techniques, such as scanning electron microscopy and histology (e.g., Webb, 1989a;Ghedotti et al, 2018), x-ray computed tomography (e.g., Schaefer, 2003;Webb et al, 2006;Schwarzhans et al, 2018), and magnetic resonance imaging (e.g., Chakrabarty et al, 2011;Graham et al, 2014), have helped identify a wealth of anatomical features that have facilitated our interpretation of fish evolution (e.g., Potthoff et al, 1986;Springer and Johnson, 2004;Hilton et al, 2015). These techniques have helped us discover, differentiate, and assess the homology and phylogenetic significance of particular anatomical features (e.g., Johnson, 1975;Gemballa and Britz, 1998), were critical for identifying characters that suggested novel placements of taxa within the broader phylogeny of fishes (e.g., Rosen and Parenti, 1981;Johnson and Patterson, 1993;Stiassny, 1993), allowed researchers to assess the intrarelationships of lineages of fishes hypothesized to be closely related (e.g., Parenti, 1981;Baldwin and Johnson, 1996;Harold and Weitzman, 1996), or aided the search for the sister group of well-established clades (e.g., Gill and Mooi, 1993;Johnson and Brothers, 1993).…”

The first evidence of intrinsic epidermal bioluminescence within ray‐finned fishes in the linebelly swallower Pseudoscopelus sagamianus (Chiasmodontidae)

“…The photophores exhibit a structure typical of many intrinsically bioluminescent taxa with overlying tissues serving as a filter or lens (Ghedotti et al ., ; Hansen & Herring, ; Lawry, ; Mallefet et al ., ; Nichol, , ; Poulsen, ). The photophores also lack the obvious bacteria‐containing chambers present in all other known bacterially bioluminescent fish taxa (Bassot, ; Chakrabarty et al ., ; Dunlap & Nakamura, ; Ghedotti et al ., ; Haneda, ; Munk, ; Okada, ; Poulsen et al ., ; Somiya, ) (Figure d,f). The continuity of the likely photogenic and overlying cells with the epidermis and the absence of any possible photogenic cells in the collagen‐rich dermis indicate an epidermal identity (Figure f).…”

“…Bioluminescent organs evolved at least 27 times in teleosts and include multiple instances of the evolution of both bacterial and intrinsic bioluminescent organs (Davis et al ., , ; Hastings, ; Herring, ). Known bacterial bioluminescent organs in fishes include a folded epithelial chamber derived from the alimentary tract or the epidermis, such as organs derived from the oesophagus (Chakrabarty et al ., ), the intestine (Dunlap & Nakamura, ; Poulsen et al ., ), the perianal proctodeum (Ghedotti et al ., ; Haneda, ; Somiya, ) and the epidermis (Bassot, ; Munk, ; Okada, ). Cases where the bioluminescent bacteria are primarily intracellular are not known in fishes (Labella et al ., ).…”

“…Epidermal involvement in photophore structure is more typical of bacterial bioluminescent organs where bacteria must be acquired from the environment, but in these cases the epidermal epithelium forms a chamber to house obvious groups of bacteria (Chakrabarty et al ., ; Ghedotti et al ., ; Munk, ; Somiya, ). Although serial photophores in other taxa may also have a developmental origin from generalised ectoderm like the epidermis, in the adult these structures are restricted to the dermis (Lawry, ; Mallefet et al ., ; Nichol, ).…”

The mitochondrial genome of Stereolepis doederleini (Pempheriformes: Polyprionidae) and mitogenomic phylogeny of Pempheriformes

“…Betancur-R et al (2017) placed Dinolestidae and Scombropidae, two families previously treated within Perciformes by Nelson et al (2016), within their Eupercaria (incertae sedis) and Scombriformes, respectively. Ghedotti et al (2018) proposed the transfer of Dinolestidae, Scombropidae, and all the families in Pempheriformes sensu Betancur-R et al (2017), excluding Percophidae, to Acropomatiformes and further expanded the order to include two new families, Malakichthyidae and Synagropidae.…”