Homology of the Fifth Epibranchial and Accessory Elements of the Ceratobranchials among Gnathostomes: Insights from the Development of Ostariophysans

Abstract

Epibranchials are among the main dorsal elements of the gill basket in jawed vertebrates (Gnathostomata). Among extant fishes, chondrichthyans most resemble the putative ancestral condition as all branchial arches possess every serially homologous piece. In osteichthyans, a primitive rod-like epibranchial 5, articulated to ceratobranchial 5, is absent. Instead, epibranchial 5 of many actinopterygians is here identified as an accessory element attached to ceratobranchial 4. Differences in shape and attachment of epibranchial 5 in chondrichthyans and actinopterygians raised suspicions about their homology, prompting us to conduct a detailed study of the morphology and development of the branchial basket of three ostariophysans (Prochilodus argenteus, Characiformes; Lophiosilurus alexandri and Pseudoplatystoma corruscans, Siluriformes). Results were interpreted within a phylogenetic context of major gnathostome lineages. Developmental series strongly suggest that the so-called epibranchial 5 of actinopterygians does not belong to the epal series because it shares the same chondroblastic layer with ceratobranchial 4 and its ontogenetic emergence is considerably late. This neomorphic structure is called accessory element of ceratobranchial 4. Its distribution among gnathostomes indicates it is a teleost synapomorphy, occurring homoplastically in Polypteriformes, whereas the loss of the true epibranchial 5 is an osteichthyan synapomorphy. The origin of the accessory element of ceratobranchial 4 appears to have occurred twice in osteichthyans, but it may have a single origin; in this case, the accessory element of ceratobranchial 4 would represent a remnant of a series of elements distally attached to ceratobranchials 1–4, a condition totally or partially retained in basal actinopterygians. Situations wherein a structure is lost while a similar neomorphic element is present may lead to erroneous homology assessments; these can be avoided by detailed morphological and ontogenetic investigations interpreted in the light of well-supported phylogenetic hypotheses.

The Gill-Arch Musculature ofProtanguilla, the Morphologically Most Primitive Eel (Teleostei: Anguilliformes), Compared with That of Other Putatively Primitive Extant Eels and Other Elopomorphs

“…Traditionally, this cartilage has been treated as epibranchial 5 (e.g., S&J), but Carvalho et al (2013) clearly demonstrated that in teleosts the cartilage develops from the distal cartilaginous end of ceratobranchial 4 and has no association with the fifth gill arch. All non-anguilliform Elopomorpha, except the albulid Albula, examined by S&J, and the highly specialized notacanthid Lipogenys (Kanehira et al, 2012) have AC4.…”

“…muscles in actinopterygian fishes. In teleosts, Ad4 attaches the posterior surface of Eb4 to Cb4 and Ad5 attaches Cb5, variously, to Cb4, AC4 (prior to Carvalho et al [2013] believed to be Eb5), ER, OP, and SO. Neither of these two muscles appears to be serially homologous with Ad1-3 or 49, which attach to the anterior surfaces of their respective Cb and Eb.…”

Phylogenetic relationships of the South American Doradoidea (Ostariophysi: Siluriformes)

“…This structure is also referred to as accessory cartilaginous nodule (Bockmann & Miquelarena, 2008: 22), and incorrectly as pharyngobranchial 1 and/or 2 (Higuchi, 1992;Birindelli et al, 2008). The term accessory element of ceratobranchial 4 is used for the small cartilage associated to ceratobranchial 4, instead of epibrancuial 5 (as in , following Carvalho et al (2013). Gas bladder terminology follows Birindelli et al (2009).…”

Ituglanis boticario, a new troglomorphic catfish (Teleostei: Siluriformes: Trichomycteridae) from Mambaí karst area, central Brazil

“…On the branchial skeleton, only the ossified elements are identified as basibranchials, and the remaining cartilaginous elements, anterior to the basibranchial 2 and posterior to the basibranchial 3 are identified as the anterior portion of copula 1 and the copula 2, respectively, according to SRINIVASACHAR (1958). Additionally, the cartilaginous element that connects the ceratobranchial 4 and 5 and the epibranchial 4 is identified as the accessory element of ceratobranchial 4 following CARVALHO et al (2013). Ray counts and symbols follow BOCKMANN et al (2004).…”