Coelacanths illuminate deep-time evolution of cranial musculature in jawed vertebrates

Abstract

Coelacanths are rare fishes that occupy a key evolutionary position in the vertebrate tree of life. Despite being exhaustively studied, we found that a substantial part of the knowledge on their cranial musculature was mistaken. Eleven previously reported coelacanth "muscles" are nonexistent, while three previously unknown muscle subdivisions and connections are found. These findings markedly affect our understanding of the deep-time cranial evolution of jawed vertebrates (gnathostomes). Only 13% of the previously identified myological evolutionary novelties for the major gnathostome lineages proved to be accurate, but several new ones are proposed. We show that low, moderate, and high levels of cranial muscle innovation characterized the emergence of lobe-finned (sarcopterygian), cartilaginous (chondrichthyan), and ray-finned (actinopterygian) fishes, respectively. The novelties in the latter group resulted in the evolution of a second active mechanism for the expansion of the oropharyngeal cavity, which was probably crucial for the predominance of suction feeding versus bite feeding in extant actinopterygians.

Fig. 1.. Cranial musculoskeletal system of African coelacanth, L. chalumnae, with associated motor branches of cranial nerves.

FMNH 76057 (CCC 59), 1070-mm total length (TL). Left lateral view with ocular muscles, facial bones, and mandibulo-hyoid ligaments removed; outlines of opercle, spiracular ossicle, and dorsal portions of sphenoidalis and rictalis represented by dashed lines. Red diamonds indicate structures unreported or erroneously reported in past studies (see the Results). CHD, constrictor hyoideus dorsalis; CHV, constrictor hyoideus ventralis.

Fig. 2.. Connection diagrams of mandibular muscles in major gnathostome lineages.

Expansor and compressor muscles in blue and red, respectively. A, adductor palatoquadrati; B, buccalis segment of AM; C, constrictor mandibularis dorsalis; D, dilatator operculi; Eth, ethmoid region; F, facialis segment of AM; Hym, hyomandibular; L, levator arcus palatini; LwJ, lower jaw; Ope, opercle (=submarginal plate in placoderms); N, sphenoidalis section of AM; O, orbitalis section of AM, P, levator palatoquadrati; Paq, palatoquadrate; PoF, postorbital fossa; PoP, postorbital process; Pro, preopercle; S, spiracularis; Spr, spiracle and/or spiracular ossicle or cartilage.

Fig. 3.. Attachment sites and reconstructions of mandibular muscles in sarcopterygians.

Actinistian L. chalumnae, (A) left lateral view of cranium [redrawn from figure 1 in (60)]. Porolepiform Durialepis edentatus, (B) medial and (C) lateral views of left palatoquadrate and dermopalatines (61) and (D) left lateral view of schematic reconstructions of mandibular muscles [skeleton based on figure 9 in (12); https://creativecommons.org/licenses/by/4.0/deed.en; endoskeletal elements in gray and separation between superficial bones in dotted lines]. Not to scale.

Fig. 4.. Attachment sites and reconstructions of mandibular muscles in chondrichthyans.

Hexanchiform Chlamydoselachus anguineus, left lateral views of (A) neurocranium, mandibular, and hyoid arches [redrawn from figure 7 in (45); https://creativecommons.org/licenses/by/4.0/deed.en] and (B) schematic reconstructions of mandibular muscles. Symmoriiform Ferromirum oukherbouchi, (C) left lateral view of the neurocranium, mandibular, and hyoid arches [redrawn from figure 4 in (39); https://creativecommons.org/licenses/by/4.0/]. Cladoselachiform Maghriboselache mohamezanei, (D) left lateral view of schematic reconstructions of mandibular muscles [skeleton based on figure 5 in (38); https://creativecommons.org/licenses/by/4.0/]. Not to scale.

Fig. 5.. Attachment sites and reconstructions of mandibular muscles in acanthodians.

Acanthodiform Acanthodes bronni, left lateral views of (A) part of braincase and (B) schematic reconstructions of mandibular muscles [skeleton redrawn from figure 4.7 in (34); https://creativecommons.org/licenses/by/4.0/deed.en]. Acanthodiform Acanthodes confusus, (C) lateral view of left palatoquadrate and lower jaw and (D) medial view of left palatoquadrate [redrawn from figure 6 in (21); https://creativecommons.org/licenses/by-nc/4.0/legalcode.en]. Not to scale.

Fig. 6.. Attachment sites and reconstructions of mandibular muscles in placoderms.

Buchanosteid arthrodire ANU V244, (A) ventral view of braincase, (B) medial and (C) dorsal views of right palatoquadrate and associated dermal plates, and (D) lateral view of left Meckel’s cartilage [redrawn from figures 3, 4, and 6 in (23); https://creativecommons.org/licenses/by/4.0/]. Arthrodiran Coccosteus cuspidatus, (E) left lateral view of schematic reconstructions of mandibular muscles [endoskeletal elements in gray and separation between superficial bones in dotted lines; skeleton based on figure 7 in (62)]. Not to scale.

Fig. 7.. Attachment sites and reconstructions of mandibular muscles in actinopterygians.

Polypteriform Polypterus bichir, left lateral views of (A) braincase and (B) suspensorium, and (C) medial view of right opercle [redrawn from figures 7, 29, and 33 in (63)]. Stem actinopterygian Raynerius splendens, (D) lateral and (E) dorsal views of left palatoquadrate and associated preopercle fragments (64). Stem actinopterygian Mimipiscis toombsi, (F) left lateral view of schematic reconstructions of mandibular muscles [endoskeletal elements in gray and separation between superficial bones in dotted lines; skeleton based on figure 101 in (32); https://creativecommons.org/licenses/by-nc-sa/4.0/]. Stem actinopterygian Australosomus kochi, (G) cross section at middle of maxillary-palatoquadrate chamber [redrawn from figure 31 in (28)]. Not to scale.

Fig. 8.. Evolutionary transformations (maximum parsimony) of cranial muscles mapped over simplified phylogenetic tree of major gnathostome lineages.

Topology based on [figure 6 in (22) and figure 11 in (27); https://creativecommons.org/licenses/by/4.0/deed.en]. Miniatures filled with gray indicate extant taxa. Synapomorphies: 1, levator palatoquadrati subdivided into levator arcus palatini and dilatator operculi; 2, CMD inserting on lateral face of palatoquadrate (10); 3, CMD inserting on hyomandibular (10); 4, presence of adductor palatoquadrati; 5, facialis originating from preopercle; 6, facialis originating from hyomandibular; 7, orbitalis originating from ethmoid region; 8, extrapalatoquadrate ridge surpassing postorbital process and coopting origin of sphenoidalis; 9, sphenoidalis originating from ethmoid region; 10, buccalis originating from neurocranium; 11, absence of CBS; 12, coracomandibularis originating from hypobranchial 3 (8, 9); more details about characters in the Results and the Supplementary Materials.

Fig. 9.. Muscular and ligamentous tissues in African coelacanth, L. chalumnae.

Details of (A) cranium showing macroscopic differences between (B) muscular (AM) and (C) ligamentous (oto-hyoid ligaments) tissues to the same scale in adult specimen (FMNH 76057, CCC 59, 1070-mm TL) and (D) histological differences between tissues in cross-sectioned embryo (AMNH 32949, CCC 29.1, RC 0727, 303-mm TL).

Fig. 10.. Branchial musculoskeletal system of African coelacanth, L. chalumnae.

FMNH 76057 (CCC 59), 1070-mm TL. Ventral view with part of left branch of sternobranchial ligament removed. Red diamonds indicate structures erroneously reported in past studies (see the Results).