Evolution of the facial musculature in basal ray-finned fishes

Abstract

BackgroundThe facial musculature is a remarkable anatomical complex involved in vital activities of fishes, such as food capture and gill ventilation. The evolution of the facial muscles is largely unknown in most major fish lineages, such as the Actinopterygii. This megadiverse group includes all ray-finned fishes and comprises approximately half of the living vertebrate species. The Polypteriformes, Acipenseriformes, Lepisosteiformes, Amiiformes, Elopiformes, and Hiodontiformes occupy basal positions in the actinopterygian phylogeny and a comparative study of their facial musculature is crucial for understanding the cranial evolution of bony fishes (Osteichthyes) as a whole.ResultsThe facial musculature of basal actinopterygians is revised, redescribed, and analyzed under an evolutionary perspective. We identified twenty main muscle components ontogenetically and evolutionarily derived from three primordial muscles. Homologies of these components are clarified and serve as basis for the proposition of a standardized and unifying myological terminology for all ray-finned fishes. The evolutionary changes in the facial musculature are optimized on the osteichthyan tree and several new synapomorphies are identified for its largest clades, including the Actinopterygii, Neopterygii, and Teleostei. Myological data alone ambiguously support the monophyly of the Holostei. A newly identified specialization constitutes the first unequivocal morphological synapomorphy for the Elopiformes. The myological survey additionally allowed a reinterpretation of the homologies of ossifications in the upper jaw of acipenseriforms.ConclusionsThe facial musculature proved to be extremely informative for the higher-level phylogeny of bony fishes. These muscles have undergone remarkable changes during the early radiation of ray-finned fishes, with significant implications for the knowledge of the musculoskeletal evolution of both derived actinopterygians and lobe-finned fishes (Sarcopterygii).

Facial and gill musculature of polynemid fishes, with notes on their possible relationships with sciaenids (Percomorphacea: Perciformes)

“…The muscles of the hyopalatine arch and the opercular series also play crucial roles in feeding and gill ventilation (Lauder, 1980, 1982; Lauder & Clark, 1984; Osse, 1969). In polynemids and sciaenids the pars primordialis of the levator arcus palatini (sensu Datovo & Rizzato, 2018) is differentiated, and in some cases even subdivided, into subsections externa and interna . The pars primordialis externa is the largest component of the levator arcus palatini , whereas the small pars primordialis interna is usually restricted to the posterodorsal region of the orbit capsule (Figures 6 and 7).…”

“…In a few polynemid species the inner portion of the primordialis section is greatly expanded anteriorly, covering most of the dorsal portion of the orbit capsule (Figures 6 and 7a). Although some differentiation within the levator arcus palatini has been documented in the literature (Datovo & Rizzato, 2018; Winterbottom, 1974a, 1993), there is apparently no reference to a similar subdivision pattern into partes primordiales externa and interna , or the extensive expansion of the latter in some polynemids. If this subdivision pattern proves to be more widespread across sciaenids, it could offer additional anatomical evidence of a close relationship between polynemids and sciaenids.…”

“…Osteological nomenclature followed primarily Johnson and Patterson (1993), as commonly used in studies on Percomorphacea. For the sake of simplicity, we use the terms facial, suprabranchial, and infrabranchial musculature as corresponding respectively to Winterbottom's (1974a) “muscles of the cheek,” “muscles serving the dorsal parts of the branchial arches,” and “muscles serving the ventral parts of the branchial arches” (Aguilera, 1986; Datovo & Castro, 2012; Datovo, de Pinna, & Johnson, 2014; Datovo & Rizzato, 2018; Howes, 1976, 1992). We highlight that these definitions, particularly “facial musculature,” are not based on muscle innervations, as commonly employed in tetrapod literature.…”

“…We highlight that these definitions, particularly “facial musculature,” are not based on muscle innervations, as commonly employed in tetrapod literature. Myological terminology follows Datovo and Vari (2013) and Datovo and Rizzato (2018) for the facial musculature and Winterbottom (1974a) for the remaining muscles.…”

“…The skeletal musculature is a system that has been traditionally neglected in most systematic studies of fishes, and those that address muscle morphologies generally have little focus on muscle homologies across different lineages (Datovo & Rizzato, 2018). However, several studies demonstrate the importance of muscles and associated connective tissues to cladistic studies (Datovo & Bockmann, 2010; Datovo & Castro, 2012; Datovo & Rizzato, 2018; Datovo & Vari, 2013, 2014; Springer & Johnson, 2004, 2015; Winterbottom, 1974b, 1993).…”