Comparative innervation of cephalic photophores of the loosejaw dragonfishes (Teleostei: Stomiiformes: Stomiidae): Evidence for parallel evolution of long‐wave bioluminescence

Abstract

Four genera of the teleost family Stomiidae, the loosejaw dragonfishes, possess accessory cephalic photophores (AOs). Species of three genera, Aristostomias, Malacosteus, and Pachystomias, are capable of producing far-red, long-wave emissions (>650nm) from their AOs, a character unique among vertebrates. Aristostomias and Malacosteus posses a single far-red AO, while Pachystomias possesses anterior and posterior far-red AOs, each with smaller separate photophores positioned in their ventral margins. The purpose of this study was to establish the primary homology of the loosejaw AOs based on topological similarity of cranial nerve innervation, and subject these homology conjectures to tests of congruence under a phylogenetic hypothesis for the loosejaw dragonfishes. On the basis of whole-mount, triple-stained specimens, innervation of the loosejaw AOs is described. The AO of Aristostomias and the anterior AO of Pachystomias are innervated by the profundal ramus of the trigeminal (Tpr), while the far-red AO of Malacosteus and a small ventral AO of Pachystomias are innervated by the maxillary ramus of the trigeminal (Tmx). The largest far-red AO of Pachystomias, positioned directly below the orbit, and the short-wave AO of Photostomias are innervated by a branch of the mandibular ramus of the trigeminal nerve. Conjectures of primary homology drawn from these neuroanatomical similarities were subjected to tests of congruence on a phylogeny of the loosejaws inferred from a reanalysis of a previously published morphological dataset. Optimized for accelerated transformation, the AO innervated by the Tpr appears as a single transformation on the new topology, thereby establishing secondary homology. The AOs innervated by the Tmd found in Pachystomias and Photostomias appear as two transformations in a reconstruction on the new topology, a result that rejects secondary homology of this structure. The secondary homology of AOs innervated by the Tmx found in Malacosteus and Pachystomias is rejected on the same grounds. Two short-wave cephalic photophores present in all four genera, the suborbital (SO) and the postorbital (PO), positioned in the posteroventral margin of the orbit and directly posterior to the orbit, respectively, are innervated by separate divisions of the Tmd. The primary homologies of the loosejaw PO and SO across loosejaw taxa are proposed on the basis of similar innervation patterns. Because of dissimilar innervation of the loosejaw SO and SO of basal stomiiforms, primary homology of these photophores cannot be established. Because of similar function and position, the PO of all other stomiid taxa is likely homologous with the loosejaw PO. Nonhomology of loosejaw long-wave photophores is corroborated by previously published histological evidence. The totality of evidence suggests that the only known far-red bioluminescent system in vertebrates has evolved as many as three times in a closely related group of deep-sea fishes.

The Complex Evolutionary History of Seeing Red: Molecular Phylogeny and the Evolution of an Adaptive Visual System in Deep-Sea Dragonfishes (Stomiiformes: Stomiidae)

“…Each included many fewer stomiid taxa than the present study, however both recovered a similar phylogenetic pattern with respect to one another in that Idiacanthus and either Stomias or Chauliodus shared an MRCA to the exclusion of Aristostomias . These relationships are incongruous with our phylogenetic hypothesis of these genera and those of the two previous phylogenetic reconstructions of the family (Fink ; Kenaley ). In addition, Hunt et al.…”

“…Within the Grammatostomias – Bathophilus + EPL clade, the outstanding differences between this hypothesis and previous studies concern the placement of Eustomias and the interrelationships of the “malacosteine” loosejaw taxa. Both the morphological studies of Fink () and Kenaley () proposed a monophyletic loosejaw + Pachystomias clade sister to a clade containing Eustomias , Grammatostomias , and Bathophilus , where our analysis supports a Eustomias + Photostomias clade nested within the a lineage comprising Pachystomias and the remaining loosejaw genera Malacosteus and Aristostomias (Fig. ).…”

“…The phylogenetic hypothesis inferred by our analysis differs in several important aspects from other phylogenetic treatments of the Stomiidae. The most notable difference is that both Fink () and Kenaley () recovered a monophyletic Stomiidae, while this study inferred a sister relationship between the stomiid Chauliodus and the phosichthyid Ichthyococcus (Fig. ).…”

“…Hunt et al. () inferred amino acid substitutions within their sparsely sampled group of dragonfishes—which did not include the red‐sensitive P. microdon , the purported sister taxon of the loosejaws (Kenaley, )—by ancestral state estimation under an unspecified optimality criterion, presumably parsimony. In addition, the topology used in Hunt et al.…”

Bioluminescence

“…A well-illustrated description of the dragonfi sh light organs and further references are provided by Kenaley ( 2010 ); Kenaley et al (2014).…”