Evolution and development of the vertebrate neck

Abstract

Muscles of the vertebrate neck include the cucullaris and hypobranchials. Although a functional neck first evolved in the lobe-finned fishes (Sarcopterygii) with the separation of the pectoral/shoulder girdle from the skull, the neck muscles themselves have a much earlier origin among the vertebrates. For example, lampreys possess hypobranchial muscles, and may also possess the cucullaris. Recent research in chick has established that these two muscles groups have different origins, the hypobranchial muscles having a somitic origin but the cucullaris muscle deriving from anterior lateral plate mesoderm associated with somites 1-3. Additionally, the cucullaris utilizes genetic pathways more similar to the head than the trunk musculature. Although the latter results are from experiments in the chick, cucullaris homologues occur in a variety of more basal vertebrates such as the sharks and zebrafish. Data are urgently needed from these taxa to determine whether the cucullaris in these groups also derives from lateral plate mesoderm or from the anterior somites, and whether the former or the latter represent the basal vertebrate condition. Other lateral plate mesoderm derivatives include the appendicular skeleton (fins, limbs and supporting girdles). If the cucullaris is a definitive lateral plate-derived structure it may have evolved in conjunction with the shoulder/limb skeleton in vertebrates and thereby provided a greater degree of flexibility to the heads of predatory vertebrates.

Fig. 1

Diagram of stage 10 chick embryo. Pink represents the head mesoderm and yellow, lateral plate mesoderm. Somites in green contribute to the hypobranchial muscles (Couly et al. 1993). The blue area indicates the lateral plate mesoderm which gives rise to the cucullaris muscle and its derivatives according to Theis et al. (2010). H, head mesoderm; L lateral plate mesoderm; O, otic vesicle; s1–s3, somites one to three; ?, indicates the uncertainty of the border between the head and lateral plate mesoderm.

Fig. 2

Eastmanosteus sp. (Placodermi; Australian Museum AMF82185). The headshield and trunkshield are ventrally and laterally separated. Originally, the shields were connected dorsally (see text) but due to damage, this region appears separated (modified from Johanson & Smith, 2003).

Fig. 3

Phylogenetic relationships of the Vertebrata (adapted from Brazeau, 2009).

Fig. 4

Muscles of the branchial and pectoral region of a shark, Scyllium canicula. The muscle in blue is derived from the cucullaris and the muscles in green are from the hypobranchial group (modified from Allis, 1917). Chy, coracohyoideus; Cmd, coracomandibularis; S, shoulder girdle; Tr, trapezius.

Fig. 5

Muscles of the neck and pectoral region of a salamander, Necturus maculosus. The muscle in blue is derived from the cucullaris and the muscles in green are from the hypobranchial group (modified from Wilder, 1912). oh, omohyoideus; rc, rectus cervicis; rhp, rectus superficialis hypobranchialis posterior; t, trapezius.

Fig. 6

Muscles of the neck and pectoral region of a bird, Cyanocorax cyanopogon. The muscles in blue are derived from the cucullaris and the muscles in green are from the hypobranchial group (modified from Fürbringer, 1902). clhy, cleidohyoideus; cuc, cucullaris and sternocleidomastoideus; cuc.1, cranial part of cucullaris; cuc.2, cervical part of cucullaris; cuc.dc, cucullaris dorsocutaneus; cuc.pt, cucullaris propatagialis.

Fig. 7

Anatomy of the neck and shoulder region of a rabbit. The muscles in blue are derived from the cucullaris and the muscles in green are from the hypobranchial group. Please note that although dsc-i, musculus dorsoscapularis inferior, is also considered to be part of the cucullaris group, there is currently no description of its development (modified from Streissler, 1900). clm, cleidomastoideus; cloc, cleidooccipitalis; dsc-s, dorsoscapularis superior; sh, tendon; stms, sternomastoideus superficialis; sth, sternohyoideus; stth, sternothyroideus.

Fig. 8

Diagram of stage 19 chick embryo, showing the cells migrating from the ventral somites into the hypoglossal chord (grey) and further anterior into the head region (modified from Hunter, 1935). H, hypoglossal chord; O, otic vesicle; p1–p3, pharyngeal pouches; s2–s4, somites two to four.

Fig. 9

Osteostraci (A) Cephalaspis lyelli (NHM UK OR 20087). The headshield is fused with the pectoral girdle and no neck region can be observed. (B) Reconstruction of a zenaspidid osteostracan (modified from Janvier, 1996).

Fig. 10

Lateral view of the head and pectoral girdle of Eusthenopteron foordi. Opercular bones have been removed to emphasize the ventral and lateral separation of the pectoral girdle from the head. Modified from Andrews & Westoll (970). Reproduced by permission of The Royal Society of Edinburgh from Transactions of the Royal Society of Edinburgh volume 68 (1970), pp. 207–329. Acl, anocleithrum; Cla, clavicle; cle, cleithrum; Pt, post-temporal bone; Scl, supracleithrum.