the development of tetrapod limb musculature — the shoulder region of lacerta

T H E DEVELOPMENT O F TETRAPOD TiIRIB hfUSCULATURE - THE SHOULDER

REGION O F LACERTA

ALFRED SHERWOOD ROMER The Biorogical Laborafories, Harvard rnicers i ty , Cambridge, Massaohusetts

EIGHTEEN FIGURES

The present paper is one of a series describing the ontogenetic development of the limb muscles of various land vertebrates in an attempt to place the comparative study of limb musculature on a firmer basis than now exists. The general scope and purposes of the work was discussed in an earlier paper (Rorner, '12, pp. 251-253, etc.) and need not be repeated here.

Below is given a description of a series of stages in the differentiation of the muscles and associated structures of the proximal portion of the pectoral limb of Lacerta agilis. As in the work cited, the material used is from the hlinot collection of Harvard University Medical School. A considerable nuni- ber of embryos was studied in preliminary fashion, and five stages selected for more detailed study. Of these the second, third and fifth were reconstructed by the wax plate method. The major processes of differentiation occur in embryos between approximately 6 mm. and 9 mm. crown-rump length. The muscle terminology employed is essentially that used previously by the writer ('22) for adult lizards.

I mi indebted to Drs. ,J. L. Breiiier and G. B. Wislocki for the use of this material. Preliminary studies, made some years ago, were aided by a grant from the research funds of the Division of Biolo,T of the University of Chicago. Completion of the work was aided by a grant from the Milton Fund of Harvard University.

1

J O U R N A L OF MORL'HOLOCY. V O L . 74. NO. 1 J A N U A R Y , 1944

2 ALFRED SHERWOOD ROMER

DESCRIPTION

Stage Z As in the case of the hind leg (cf. Romer, '42, pp. 253-254)

a first definite stage in differentiation is seen in embryos of 5-6 mm. crown-rump length. The limb bud a t this stage contains three layers of mesenchyme, arranged dorso-ventrally, the central layer being that of the potential limb skeleton, the upper and lower ones sheets of premuscular tissue which represent the future dorsal and ventral muscle masses. These premuscular tissues are believed by hIollier (1895) to be of myotomic origin in Lacerta. However they are at this time quite distinct at ahnost all points from the myotomes, and from this time onward pursue a history independent of those structures. The dorsal and ventral premuscular masses are simple lobate structures ; their outlines a re not clear-cut and hence three-dimensional reconstruction is unprofitable. Their appearance as seen in section is well illustrated by Mollier (1895, pls. XXX-XXXVI).

Stage IZ EMBRYO NO. 814, MINOT COLLECTION. CROWN-RUMP LENGTH

6.4 MM. (FIGS. 1-6).

SkeZetouz. Girdle and limb skeleton a re represented by a mass of condensing mesenchyme in which all but the more distal regions can be readily identified; the elements are, however, very short and there are no lines of demarcation between them. I n the shoulder region a thick mass of tissue is present in the future glenoid region. Ventrally the tissue is also thickened in the coracoid region and map include the material of the future sternum. The mesenchyme has extended ventro- anteriorly to enclose the supracoracoid nerve in a coracoid foramen. The two halves of the girdle a re remote from one another, and there a re no indications of dermal elements.

The region of the future humerus is a short but very broad area of condensed mesenchyme extending from the girdle to the future elbow region. Proximo-laterally near the presumed

DEVELOPMENT O F SHOULDER O F LACERTA 3

head of the humerus are two pronouiiced lateral “tuberosi- ties” of mesenchyme which are at first sight difficult of interpretation. These undergo gradual relative reduction in later stages. The more distal of the two becomes the adult ddto- pectoral crest of the humerus ; the more proximal appears to represent the anterior buttress of the glenoid cavity. The adult humerus lacks the entepicondylar foramen which in primitive reptiles encloses the ulnar nerve. This structure, however, is present in mesenchyme a t this stage ; it disappears later.

Radius and ulna are represented by a pair of mesenchymal masses extending from the presumed elbow into the distal portion of the limb bud. Seemingly irregular swellings on both (but more highly developed on the ulna) represent the future carpal and digital regions.

Nerves. The nerve plexus is already well formed and the nerves are a t this stage relatively large structures. Post- cranial nerves VI-IX take part in the formation of the plexus. Nerves VI and VII (the first the smallest of the four) unite

ABBREVIATIONS

Bi, biceps Bri, brachialis inferior Cb, coraco-brachialis Cbb, coraco-brachialis brevis Cbl, coraco-brachialis longus C1, clavicle Cor, coracoid Dcl, deltoides clavicularis DSC, deltoides scapularis Ect, ectepicondyle Ent, entepicondyle Ext, extensors of forearm Fect, ectepicondylar foramen Fent, entepicondylar foramen Flex, flexors of forearm H, humerus Hr?, tissue probably representing

Hum, humerus Icl, interclavicle

humero-radialis muscle

Ld, latissimus dorsi Lsch, seapulo-humeral ligament N cut, cutaneous nerve N med, median nerve N rad, radial nerve N spc, supracoracoid nerve N uln, ulnar nerve Olee, olecranou P, pectoralis Rad, radius Sbc, subcoracoideus Sbcsc, subcoraco-scapularis Sbsc, subscapularis Sc, scapula Sclia, scapulo-humeralis anterior Spc, supracoracoideus St, sternum Ti., triceps Uln, ulna TI-IX, spinal nerves

4 ALFRED SHERWOOD ROMEK

close to their roots and give off, before reaching the plexus proper, the supracoracoid nerve. This passes downward on the inner surface of the girdle, passes through the coracoid (supracoracoid) foramen and reaches the most anterior portion of the ventral muscle mass.

In the main portion of the plexus two iiiaiii trunks are discernible, one antero-dorsal in position and lying above the head of the humerus, the other ventral and posterior along

Fig. 1 Stage 11. The skeleton and nerves of the right pectoral limb in lateral view. Girdle and limb form a single unbroken mass of pre-cartilaginous tissue; the dermal girdle has not appeared. The nerves a re relatively large. I n this and later figures the labels on many of the terminal branches refer to the muscles supplied.

VI VII VIII IX

N

Fig. 2 Stnge 11. A s in figure 1; medial view.

DEVELOPMENT O F SHOULDER OF LACERTA 5

the inner (posterior) surface of the humeral head. Seemingly all four nerves contribute to both trunks, but nerves VI-VII are mainly concerned with the anterior trunk and nerve IX contributes most of its fibers to the posterior trunk. These trunks are associated respectively with the two muscle masses, dorsal and ventral, present at this stage. The antero-dorsal trunk innervates, by various branches, the more proximal portions of the dorsal muscle mass. A prominent cutaneous nerve emerges onto the lateral (anterior) surface of the brachial region. The radial nerve is (as in all lizards) relatively small and short and does not extend beyond the knee region.

The postero-ventral trunk is associated primarily with the ventral muscle mass. Short branches supply the proximal portion of this mass. Distally ulnar and medial nerves are present. The former passes down the posterior surface of the prospective humerus and through the mesenchymal equivalent of the entepicondylar foramen. From there it runs downward along the ulna beneath the premuscular tissue of the ulnar part of the future flexor musculature. The medial nerve takes a more ventral course, and runs downward beneath the central part of the future flexors. Even at this stage there is present an interosseous branch of this nerve passing upward between radius and ulna (as in lizards generally) to supplant the radial nerve as the source of innervation of the extensor musculature of the forearm and manus.

Musculuture. The future musculature is at this stage still in the general condition seen in stage I - that is, in two distinct premuscular masses, dorsal, and ventral. The two are nowhere in contact and at almost every point widely separated from one another-this in contrast to the adult condition where muscle growth has brought various derivatives of the two masses close to one another. Each mass is still a single, unified structure, although the first stages of differentiation are already patent. For the most part both masses are quite distinct from the axial musculature. The only exception is that postero-ventrally there is a small area of the ventral mass

6 ALFRED SHERWOOD RO'MEB

(in the region of the future pectoralis) which is close to the myotome posterior to nerve IX and may be continuous with it:

The dorsal mass covers the upper surface of the future humerus and the adjacent region of the girdle and extends downward as a lobate structure over the future extensor surface of the forearm. While all parts of the mass are in connection with one another, the beginnings of subdivision into several groups are already apparent. The areas between these

Ld + Sbcsc

Fig. 3 Stage 11, the right pectoral limb in dorsal view. The dorsal muscle mass is shown, together with the more postrro-lateral portion of the ventral mass. Although the two masses of premuscular tissue are still units, the general areas from which the future discrete muscles arise can be roughly determined and are labeled.

subdivisions are in general relatively thin bands of more diffuse tissue. Proximally and internally a thickened area is present which is seen in later stages to give rise to the latissimus dorsi and subcoraco-scapularis muscles. Antero-laterally there is an area from which the deltoid muscles are the main derivatives. Above the humerus, more posteriorly, is a thick lump of tissue, the adage of the triceps (anconaeus) ; this and the last are separated by a broad cleft. Distally the future extensor musculature forms a broad sheet above the radius and ulna ; proximally there are slight evideiices of the future subdivisions of the extensors.

7 DEVELOPMENT OF SHOULDER OF LACERTA

The ventral mass is more irregular in shape and does not as readily analyze into future coinponents. I n some regards it is comparable with the structure of the ventral mass as seen in early stages of the pelvic limb of Lacerta (cf. Romer, '42, fig. 5, etc.). Proximally the mass is broadly expanded. An exterior thickened area (into which the supracoracoid nerve enters) represents the future supracoracoid muscle. Poster- iorly and medially a larger and thicker area is the anlage of the pectoralis (as noted above this is still in contact at its

Fig. 4 Stage 11. As in figure 3, but a-lateral view. In addition to the dorsal muscle mass, the margin8 of the ventral mass a.re visible both dorsally and ventrally.

Fig. 5 Stage 11. As in figures 3-4, but a ventral view. The ventral muscle mass is displayed, but the lateral margin of the dorsal mass is seen at the 10WCT

margin of the figure.


posterior tip with the axial musculature). Between these two areas (and somewhat more distally situated) is the region from which coraco-brachialis, brachialis and biceps appear to originate. Distally the future flexor musculature extends in lobate fashion down over the under surface of radius and ulna. This flexor musculature is still broadly connected u7ith the more proximal groups. However (as in the case of the extensors) tbe future subdivisions are already in evidence to some degree.

Fig. 6 Stage 11. As in figure8 3-5; a medial view, showing the ventral muscle mass and the dorsal margin of the dorsal mass.

Stage IZI EMBRYO 814. CROWN-R,UMP LENGTH 7.4 MM. (FIGS. 7-10)

Skeleton. The outlines of the future endochondral elements, present in a precartilaginous stage, are less diffuse than in stage 11, and much of the girdle and limb skeleton is assuming recognizable shape, although the elements are short and continuous with one another. The primary shoulder girdle pre- sents a recognizable scapular blade, a thickened glenoid region in which the antero-lateral buttress (so prominent in stage 11) is somewhat reduced, and a broad coracoid plate, extending fa r below the coracoid foramen. Considerable progress is seen in the development of a sternal plate. As fa r as could be determined the plate is not connected with the ribs, and since the two girdles are still far removed from one another, it is

DEVELOPMENT OF SHOULDER OF LACERTA 9

developing as a paired structure. The clavicle is already in process of formation, but no evidence of an interclavicle is as yet apparent. The humerus has lengthened, and the general contours of the mature bone can be made out. The delto- pectoral crest is prominent. No entepicondylar foramen is present, the mesenchyme which surrounded the ulnar nerve in the last stage having failed to keep pace with the general

Fig. 7 Stage 111, the skeleton and nerves in lateral view.

Fig. 8 Stage 111, tlir skeleton and nerves in medial view.

10 A L, FRED S H EBR’OOD EiOMER

Fig. 9 Stage 111, tlie limb in lateral view. For comparable earlier and later stages see figures 4 and 11. Gross differentation of future muscle groups is under way. Histological differentiation is little advanced. Areas in which myogenesis is not taking place a re represented by coarse stipple; these include an area (HrB) on the lateral border of the humerus coniparable t o that occupied by the humero- radialis muscle of other reptiles.

Fig. 10 Stage 111, tlie limb iii mediril view. For eoiliparal~le earlier and later stages see figures R and 13.

DEVELOPMENT OF SHOULDER O F LACEHTA 11

growth of the limb. There is a prominent ectepicondyle, but I fail to find an associated foramen.

The more distal portion of the limb was not studied in detail but, as can be seen, formation of the carpal region and phalanges is well advanced.

Nermes. The nervous elements have elongated, in correla- tion with other organ systems. The same general distribution can be discerned as in stage 11. The dorsal trunk noted in that stage is apparently tending to divide into an anterior portion iiicluding the nerves to the deltoid region and the lateral cutaneous nerve, and a posterior group including nerves to latissimus and triceps and the rudiment of the radial nerve. Ventrally both ulnar and medial nerves to the lower part of the limb are much farther advanced, but the distribution of branches to the more proximal muscles is similar to that seen in stage 11.

Musculature. The tissues are here in a pre-muscular stage. The outlines of the muscles and muscle groups are more sharply defined than in stage 11, but little advance has been made in histological differentiation.

The musculature here is at an interesting stage in gross development. The two muscle masses visible earlier are still essentially units ; all portions of the dorsal and ventral masses are still in contact with adjacent regions of the same mass, and dorsal and ventral masses are clearly separable. But within each of the two masses there are clearly marked local developments in which (particularly proximally) the anlagen of many of the adult muscles can be readily identified. Be- tween these various anlagen are thinner bands of tissue which disappear, for the most part, in later stages.

In the dorsal group an anterior region, that of the future deltoids + scapulo-humeralis anterior, was already discernible in stage 11. Here this muscle group is nearly completely separated from its neighbors and has expanded to some degree over the scapula, both dorsally and anteriorly toward the clavicle. A split in its distal margin suggests the future cleavage between clavicular deltoid and scapular deltoid


(dorsalis scapulae), but no indication of a separate scapulo- humeralis anterior is apparent.

In stage I1 there was seen a semi-distinct dorso-medial area of the dorsal mass. Here this has divided into two portions. From this region there has grown up a thin sheet of tissue extending antero-posteriorly in the general plane of the scapular blade but posterior to it, as the latissimus dorsi. A more medial and ventral portion of this area has grown inward beneath the nerve plexus and over the margin of the glenoid region of the girdle to form the subcoraco-scapularis which is, however, little expanded at this stage. Distal to the latissimus a stout band of premuscular tissue extends to the neighbor- hood of the future knee joint as a rudimentary triceps.

In stage I1 the future deltoid region was in connection at its lower end with the more distal portion of the dorsal mass through the medium of a band of tissue running to the lateral margin of the future triceps. Essentially this condition is retained in the present stage. A prominent band of tissue extends from the deltoid group downward along the lateral margin of the triceps to the elbow region. Unlike the adjacent portion of the triceps, this band of tissue shows no indications of myogenic development and apparently disappears in later stages. It is suggested below that this band may be analogous to the humero-radialis muscle, absent in Lacerta but present in certain other reptilian forms.

The distal portion of the dorsal muscle mass is still connected with the proximal portion, but is undergoing rapid development and morphological differentiation. This region, however, has not been studied in detail and is not further considered here.

In the ventral muscle mass the supracoracoideus muscle is partially separated from its neighbors. Much of the remainder of the proximal part of the ventral mass forms a sheet arising from the coracoid plate extending out along the undersurface of the humerus and laterally reaching the ulna. The coraco- brachialis and biceps are derivatives of this sheet but are as


yet incompletely differentiated. At its dorso-lateral margin the brachio-radialis i s already partially distinct.

In stage I1 a thickened area of the ventral mass extended posteriorly and medially. This develops as the pectoralis, here separated off though incompletely from the deeper ventral sheet. It appears to be growing rapidly posteriorly, external to the sternum, and is also expanding anteriorly. Toward its anterior end it is also extending upward over the deep sheet toward its definitive insertion the delto-pectoral crest; however its coiinectioii with this process is as yet a tenuous one.

The distal portion of the ventral mass is also undergoing marked development. It has not, however, been studied in detail and will not be considered in later stages.

Stage ZV EXBRYO NO. 810. CROWN-RUMP LENGTH 7.9 MM. (FIGS. 11-13)

This stage has not been reconstructed in three dimensions, but studied in sections and in graphic reconstruction. Histo- logical differentiation is far advanced, although the embryo is but little larger than that of stage 111. The primary girdle and major limb bones are already formed in cartilage, for the most part. The tissues of the future muscles have in great measure become typical muscle fibers. The nervous system was not studied in detail and is not figured.

Skeleton. The two halves of the girdle are still widely separated ventrally ; the clavicles fade out into connective tissue on the under surface of the neck and there is as yet no interclavicle. The scapulo-coracoid has essentially the adult form, except that the fenestrae seen in the adult have not as yet been formed into the coracoid plate. Sternal ribs are present, but are not attached closely to the sternum (and are not shown in our figures). A small ectepicondylar foramen is present in the humerus. A definite olecranon is present. The distal portion of the limb was not studied.

Musculature. Further differentiation of the individual muscles has taken place, particularly in the dorsal group. In


stage I11 the future deltoid region showed but a single muscle with only slight evidences of subdivision. Here the inseltion area is still single ; but distally there are three distinct muscles : clavicular deltoid, scapular deltoid (dorsalis scapulae), and (deep to the others) scapulo-humeralis anterior. The scapular deltoid already exhibits the partial subdivision distally which is characteristic of the adult Lacerta.

Fig. 11 Stage IV, the limb in lateral view. For comparable earlier and later stages see figures 9 and 16. The distal musculature has become nearly completely separated from that of the shoulder region and ie not shown in this and later figurea.

The subcoraco-scapularis has expanded further on the internal surface, and future scapular and coracoid portions (separated by the supracoracoid nerve) can be distinguished. The latissimus dorsi is expanding rapidly. The triceps is still a single mass, in which the quadripartite adult division of the heads is not apparent. The mass of condensed tissue whicb was described in stage I11 as passing down the lateral margin of the humerus from the deltoid region, between triceps and brachio-radialis is present but apparently has retrogressed and is more diffuse ; it is not figured.

15 DEVELOPMENT OF SHOULDER OF LACERTA

Ventrally, differentiation is still incomplete. The pectoralis has undergone considerable expansion posteriorly, external to the sternum and sternal ribs. Close to its insertion, the pectoralis is still difficult to separate from the underlying muscles (coraco-brachialis and biceps). The supracoracoideus is quite

n

Fig. 12 Stage IT, the limb in lateral view to show the deeper musculature. The deltoids, latissimus dorsi and triceps have been removed and the humerus and its ventral musculature sectioned.

/-- <

Fig. 13 Stage IV, the limb in nicdial view. For comparable earlier and later stages see figures 10 and 18.


distinct near its insertion, but close to the coracoid is difficult to separate from the adjacent coraco-brachialis. Proximally coraco-brachialis longus, biceps and brachio-radialis have heads distinct from one another and froin the coraco-brachialis brevis ; part way down the shaft of the humerus, however, the boundaries are still more or less indistinct.

The musculature of the forearm was not studied. Connec- tions still exist to some extent between triceps and extensor forearm musculature and between biceps and flexors but have been omitted from the figures for purposes of simplification.

Stage I.' EMBRYO NO. 1602. CROWN-RUMP LENGTH 9 Mhl. (FIGS. 14-18)

Skeleton. The form of the girdle and limb elements is already essentially that of the adult; these structures, however, are still in a cartilaginous condition. The two girdles have at length approached each other ventrally, and the interclavicle has appeared along the ventral midline. Fenestrae underlying scapulo-humeralis anterior and supracoracoideus muscles have already appeared in the fornierly solid plate ventral and anterior to the glenoid. The sternum is now 8 single well formed structure and clasps closely the postero- ventral margins of the coracoid; the sternum and sternal ribs are in close apposition. At both ends of the humerus well- formed joints are present. Proximally there is already formed the complex set of ligaments connecting scapula with humerus and coracoid well described in adult lizards by Furbringer ('00, figs. 133-158 etc.), except that the condition seen is rather closer to that shown for Zonurus or Zonosaurus than for that figured by Furbringer for the adult Lacerta. The ligaiiients form a sheath through which runs the scapulo-1iaIneralis anterior muscle; from them arises the scapular head of the triceps.

Nervozis s~ystem. The nerves are not well stained in this specimen and it is possible that the description given below contains omissions and inaccuracies in regard to the distribu-


tion of the finer branches. With elongation of the limbs the pattern of the nerve plexus and the nerve branches is essentially that of the adult. Nerves VI and VII unite internal to the upper part of the scapular blade and before entering further into plexus formation give off a branch ventrally to the subcoraco-scapularis and a parallel, much larger supracoracoideus nerve. This last separates two portions of the

B N

Fig. 14 Stage V, lateral view of the shoulder girdle and nerves.

subcoraco-scapularis muscle and, descending beneath this muscle, traverses the coracoid foramen to the supracoracoideus muscle and the skin of the supracoracoid region. Also formed in great measure, if not entirely, from nerves VI-VII are the branches which innervate the two deltoid muscles.

More distally, close to the posterior margin of the scapular deltoid near its lower end, the main trunk descending from roots VI-VII is joined by a component from VIII-IX to form a short lateral nerve trunk. Froin this arises a small branch to the scapulo-humeralis anterior, a cutaneous nerve to the


lateral surface of the upper arm, and branches which innervate the various divisions of the triceps. As noted earlier, the radial nerve is reduced and I have been unable to trace any remains of it beyond the region of the triceps, although there persists a small ectepicondylar foramen.

A much larger nerve trunk is that formed internal to the lower portion of the latissimus dorsi muscle. Into this pass all fibers from nerves VIII-IX (except the small contribution

Fig. 15 Stage V, medial view of the shoulder girdle and nerves.

to the lateral trunk noted above) and also a strong comple- ment of fibers from nerves VI-VII. From this trunk are derived short but strong branches: one to the pectoralis passing ventrally between coraco-brachialis longus and coraco-brachialis brevis, and a second branch to the latter muscle and the proximal head of the biceps (this last branch turning ventrally close to the medial margin of the glenoid). The median trunk gives rise to the large ulnar and median nerves, which pass down the arm close together and between coraco-brachialis longus and triceps. Distally they diverge, the uInar nerve


emerging to the surface dorsally and medially in the region of the entepicondyle, the median nerve taking a more ventral course to the radial side of the flexor surface of the forearm. The fibers innervating brachialis, coraco-brachialis longus and the distal belly of the biceps accompany the median nerve.

Musculature. The musculature is in an essentially adult condition. Both histological and gross morphological differentiation have been completed.

Fig. 16 Stage V, lateral view of the shoulder musculature. For comparable views at earlier stages see figures 4, 9, and 11.

Of the dorsal muscles, the primitive “deltoid” group is separated clearly into three conipoiients. The scapular deltoid (dorsalis scapulae) arises from the outer surface of the scapular. blade; it is partially divided distally into two portions. The clavicular deltoid arises from the clavicle, from its inner surface and froill its outer surface by a mass of tissue which wraps itself around the anterior margin of the bone. Near their adjacent intersections on the delto-pectoral crest there


is an exchange of fiber-bundles between the two muscles. The remaining derivative of the primitive deltoid group - sap - ulo-hurneralis anterior - arises from the area of the scapular fenestra and runs backward, covered by the deltoids, through a tent-like sheath formed by the scapulo-humeral ligaments.

The latissimus dorsi has continued its expansion into the adult condition of a greatly developed thin sheet covering

- I - - B i t Cbb

Fig. 1 7 Stage V. As in figure 16, but with the more superficial muscles removed and the humerus and adjoining nerves and muscles seen in section. Com- pare figure 12.

much of the lateral surface of the thoracic region, with its fibers converging to a tendon which inserts between the two long heads of the triceps. The subcoraco-scapularis now covers most of the inner surface of the primary girdle, forming a great fan-shaped structure, the fibers of which coiiverge to insert near the medial border of the head of the humerus. The iriuscle is divisible into two major portions, the point of division being that at which the supracoracoid nerve passes


onto the surface of the girdle on its way toward the coracoid foramen. Dorsal to this is the subscapular portion of the muscle, its major portion being a stout band of tissue running diagonally downward and backward from the inner surface of the upper part of the scapular blade. A considerable mass of fibers arises from the posterior margin of the scapular blade.

Fig. 18 Stage V, medial view of the shoulder musculature. For comparable earlier views see figures 6, 10, and 13.

These, however, do not extend to any marked degree to the outer surface (and are hardly to be considered as a separate scapulo-humeralis posterior muscle).

The part of the muscle below the point of entrance of the supracoracoid nerve may be termed the subcoracoideus (although part of its area of origin lies on the inner surface of the future scapula). Much of its extent consists of a relatively thin sheet of tissue; its more dorsal portion, however., is more strongly developed.


The triceps, a single mass when last seen, has attained its definitive condition by proximal growth and subdivision. Medial and lateral humeral heads are apparent. In connection with the former is a slender tendon - the coracoid head - which arises on the inner surface of the coracoid and passes outward on to the limb lateral to the median nerve trunks. The scapular head arises from the scapular-humeral ligament s y s tem.

At this stage there is no trace of the band of tissue noted earlier as lying lateral to the triceps.

I n the ventral musculature the pectoralis is weil developed as a great sheet of tissue covering superficially the entire ventral aspect of the girdle region and extending backward over the surface of the sternum and anterior abdominal region. The fibers converge to a well developed tendon which inserts on to the delto-pectoral crest. The snpracoracoidens, covered superficially by clavicular deltoid and pectoralis, has expanded over the large area of the coracoid where the coracoid fenestra has developed in connection with it. Proximal and distal heads of the biceps are well developed; the intermediate tendinous portion, however, is not too clearly distinguishable from the underlying coraco-brachialis brevis. Proximally the brachidis is quite discrete, lying along the lateral rriargin of the humerus. Distally, however, brachialis and biceps become closely associated and there is some interchange of fibers, although the biceps is mainly ulriar in its insertion, the hrachialis radial.

Coraco-brachialis brevis and longus are quite distinct at their origins, the former arising broadly from the ventral or external surface of the coracoid, the latter from a small area on the internal surface of the coracoid near its posterior margin. The areas of insertion of the two are also discrete, the former inserting ventrally on to the ventral surface of the humerus, the latter on to a more distal and medial portion of the bone. Near the insertion of the shorter muscle, the two are adjacent but for the most part clcnrly separated by the intervention of the median nerve.


No connections remain between the muscles considered here and the musculature of the forearm.

DISCUSSION

Gelzeral consideratiovz of developmental history. As shown in the preceding description, the differentiation of the pectoral limb musculature of Lacerta is a well-ordered process, highly comparable to that previously described in the case of the pelvic limbs of Lacerta and the chick. There are first established two primary masses, dorsal and ventral (extensor and flexor), lying on opposite sides of the developing limb skeleton. The distal portions of each mass undergo differentiation into the various muscles of the forearm and manus and at the same time are gradually separated from the more proximal muscles. In the proximal region, with which we are here concerned, there occurs between the 6-mm. and 9-mm. stages, a rapid differentiation of individual muscles within both dorsal and ventral masses. This process of cleavage may be diagrammatically represented as follows :

Dorsal muscle mass

Ventral muscle mass

Proximo- medial group

Proximo- lateral (axillary) group

Triceps

( Peetoralis

Lat.issimus dorsi

8ubcoraco-scapularis

Scapular deltoid Clavicular deltoid

Seapulo-liuineralis anterior

Supracoracoideus

Coraeo-brachialis longus Coraco-brachialis brevis Biceps (proximal head)

Biceps (distnl hcadj

Rrarbialis

Lateral distal

. group

24 ALFRED SHERWOOD ROME€&

I have previously discussed the relation of this type of ontogenetic process to the phylogenetic history of the musculature concerned (Romer, '42, pp. 277-279). I n view of previ- ous experience it may be confidently assumed that the situation seen here is representative, in great measure at lead, of the general phylogenetic history of the muscles involved.

The writer ('22, '24) pointed out that the pectoral limb of tetrapods had apparently been derived from a fish fin in which the relatively simple musculature was arranged in opposed dorsal and ventral masses, and attempted to classify the limb musculature of land vertebrates, in accordance with this history, into dorsal and ventral groups. As origiiially proposed, the dorsal group derivatives in lizards were believed to be the latissmius dorsi, subcoraco-scapularis, triceps, and the more distal extensor muscles, while ventral derivatives were thought to include scapular deltoid, clavicular deltoid, scapulo-humeralis anterior, pectoralis, supracoracoideus, coraco-brachialis brevis and longus, biceps, brachialis and the more distal flexors.

I n most respects this theory gained general acceptance as, for example, in Howell's excellent series of papers on the evolution of the shoulder architecture (Howell, '33, '33a, '35. '36, etc.). In one important respect, however, there has been disagreement, namely the phylogenetic history of the first three of the muscles which the writer had assigned to the ventral group - the two deltoids and scapulo-humeralis anterior (cf. Miner, '25, pp. 230-238, partim). There has been, in the pectoral appendage, a tendency for a rotation of otigin- ally ventral elements upward into a dorsal position. The writer's demonstration that the supra- and infrasp natus muscles of mammals are ventral muscles rotated to a dorsal position is, I think, generally considered as valid. The thesis that the deltoid group had undergone a similar but earlier rotation from a ventral to a dorsal situation has not met with as much favor, although backed by arguments which at the time seemed convincing to the writer ( '22, '24).


The present work shows that this last thesis, although attractive, is quite incorrect. As we have seen, the deltoid group, even though separating early in ontogeny, is an integral part of the dorsal muscle inass. I n other regards the embryological story of muscle development in ‘Lacerta agrees well with the assumed phylogeny, and the writer is willing to accept the verdict of ontogeny against him in this particular : the scapular and clavicular deltoids, and the associated scapulo-hunieralis anterior are dorsal rather than ventral muscles. The writer’s earlier tabulations of muscular arrangement and homologies are therefore subject to revision in this regard.

The embryology of the pectoral limb shows, as was true in the case of the pelvic limb, the sharp distinction between the true limb musculature and that of the axial system In discussions of limb musculature it is frequently assumed that various muscles which run from trunk to girdle-such as levator scapulae and serrati (or even trapezius) - are limb muscles. The writer has earlier pointed out that even on the basis of adult structure alone these elements are not part of the limb musculature but specialized portions of the axial musculature. The present study demonstrates this fact eni- bryologically. As we have seen, the true limb musculature separates at a very early stage from that of the trunk, and the limb bud premuscular material takes no part in the formation of levator, serrati, etc.

It is a frequent practice to classify limb rnusdles into “extrinsic” elements - those arising from the trunk- and “intrinsic” ones - those confined to the limb and girdle. The situation in the lizard pelvic limb afforded evidence that this distinction is an artificial one (Romer, ’42, p. 288). This is also the case in the pectoral limb. The latissimus and pectoralis are muscles acting on the limb but arising from the body and hence are frequently classed as “extrinsic”. As we have seen, however, these two muscles are as purely appen- ciicular as any other limb elements. The latissimus is not in contact at any early stage with the axial musculature; its

26 ALFRED SHERWOOD ROMEB

growth is from limb to body, not the reverse. The pectoralis, we have noted, has a slight contact with the axial area at an early stage, but even so there is no evidence that there is any growth of material at this stage out from the myotomes into the pectoralis; the posterior tip of the ventral muscle mass of the limb seems merely to have been somewhat retarded in its separation from the myotome system.

It is of interest to compare the ontogenetic history of the lizard pectoral musculature with the scheme of classification proposed by Howell ( ’36,36a) on the basis of a comparison of adult types. This is, in outline, as follows :

Dorsal division

[ Dorm-scapuhr group - serratus anterior, levator scapulae

Thoracodorsal matrix - latissimus, ? subcoraco-scapularis. Axillary matrix - deltoids, scapulo-humeralis anterior, B subcoraco-srapularis.

Brachial group - triceps antibrachial group

1 shoulder group

I elbow matrix

wrist matrix

f Itif razonal group - costoscapularis, sterno-coracoideus

1 [ Pectoral complex I

Procoracoid (or anterior coracoid) matrix - shou’aer group supra-coracoideus

Coracoid matrix - coraco-brachialis

Brachial group - brachialis, biceps

Ventral 1 I division

I Antibrachial group elbow matrix

1 wrist and manus groups

In two features there is marked divergence between this scheme and the ontogenetic picture; in every other respect. the two systems are in reiriarkedly close agreement.

It is, I think, clear from the developmental history that the first group in both dorsal and ventral divisions - dorso- scapular group, infrazonal group - should be removed from


consideration with the limb system. As noted above, the muscles contained in these groups have no connection at any stage with the muscle masses of the developing limb. I have not studied their development in detail, but they appear to arise as portions of the axial musculature adjacent to the girdle and differentiated for use in connection with that structure. They should properly be classified with the axial muscles.

Those muscles of the upper arm which insert distal to the elbow joint - triceps above, brachialis and biceps below - are grouped by Howell with the forearm muscles in dorsal and ventral “elbow matrices”. This does not agree with the ontogenetic story, for the first sharply established cleavages in both dorsal and ventral masses are those at the elbow region between triceps and forearm extensors and, ventrally, between brachialis plus biceps and the forearm flexors. Howell recognizes this distinction to some extent, for both dorsally and ventrally he subdivides the elbow matrix into brachial and antibrachial groups. If , in Howell’s scheme, the term “elbow matrix” were eliminated and brachial and antibrachial groups raised to independent status, the classification would agree with the developmental picture.

Once the two proposed changes are made, it is seen that the two tabulations, by Howell and the writer, are in almost perfect agreement, despite the fact that they have been formu- lated independently and on quite different bases. The proximo- medial group of the embryonic dorsal mass is equivalent to Howell’s thoracodorsal matrix, containing the la t i ssbus and subcoraco-scapularis ;l my proximo-lateral embryonic group is Howell’s axillary matrix; the triceps is a unit in itself in both systems. Ventrally, both schemes recognize four units in the shoulder and upper arm region: (1) pectoralis (Howell’s pectoral complex), (2) supracoracoideus (his procoracoid matrix), (3) the coraco-brachiales (coracoid matrix), and (4) brachialis and biceps.

1 In his discussion of Iguana ( ’36, p. 198) he tends to include the latter muscle in the axillary group, but in his paper on muscle classification ( ’36a) places its mammalian equivalent (correctly, I believe) in the thoraco-dorsal matrix.

28 ALFRED SHEBWOOD ROMER

Adult lizard musculature. The embryological history throws some light on adult lacertilian conditions and variations in limb musculature in that group.

In many lizards (as in Lacerta) the scapular and clavicular deltoids are quite distinct at their origins; since the same situation is found in forms as divergent as crocodilians and urodeles, there has been a general tendency to assume that the primitive reptile possessed a scapular deltoid (dorsalis scapulae) distinct from the clavicular deltoid. It must, however, be pointed out that the deltoid group appears to have originated as a sheet of musculature arising from the posterior margin of the dermal girdle elements, cleithrum and clavicle. Primitively these elements afforded a continuous line of origin for the deltoids along the entire anterior margin of the girdle, and it is reasonable to assume that under such circumstances the two deltoids formed a single unbroken sheet in ancestral tetrapods. This primitive condition of the dermal girdle was present not only in early amphibians, but also in early reptiles, most of which retained a oleithrum. With loss of the cleithrum in later forms among both amphibians and reptiles, modification of the dorsal portion might be expected as its origin shifted to the scapula. There is further in both urodeles and crocodilians a loss of the clavicle, inviting modification of the original clavicular deltoid. In lizards, despite the loss of the cleithrum, there are still cases, as noted by Fiirbringer ( '00, p. 428) in which the two deltoids are still united, and Rabl ( '16, p. 685-686) considers the two to form a single muscle. As we have seen, the two are a unit until a late stage in development.

The subcoraco-scapularis is slow, ontogenetically, to expand over the inner surface of the girdle ; this is in agreement with the fact that in primitive tetrapods the girdle is so con- structed that penetration of this muscle to the true inner surface of the coracoid was an impossibility (Romer, '22, p. 530; Miner, '25, p. 243; Howell, '36, p. 199). Apparently the condition seen in Uromastix (Fiirbringer, 1876, p. 738, pl. 24, etc.), in which the subcoraco-scapularis expands widely

DEVELOPMENT OF SHOULDER O F LACERTA 29

on the external surface of the scapula, is relatively rare among lizards, although repeated in Sphenodon.

The scapulo-humeralis anterior has been held to be closely related to the deltoid, essentially a deep portion of that muscle (Miner, ’25, p. 236 ; Howell, ’36, p. 198). This is confirmed by the developmental story; it appears to be especially related to the clavicular portion of the deltoid group. Embryologically it arises perfectly separated from the supracoracoideus, and the occasional tendency for approximation or fusion of the margins of these two muscles is undoubtedly a secondary con- di tion,

The descriptive term “teres” is used in mammalian ana- tomy for certain muscles arising from the posterior margin of the scapular blade and descending to insert near the head of the humerus. This term has been applied on various occa- sions to muscles in the same area in lizards and other lower tetrapod groups. Care must be observed in such a use of the term, however, for a muscle in this region may have originated in any one of four possible ways :

1. By the attachment to the posterior margin of the scapular blade of fibers from the anterior part of the latissimus, which passes close by this surface. The mammalian teres major appears to have been derived in this way. A similar structure is reported in certain lizards ( Furbringer, 1876, pp. 737-738; ’00, p. 435), and the crocodiles have a teres major of the same sort. It is probable that these are parallel developments.

2. By a movement posteriorly of part of the scapular deltoid. As fa r as I am aware this has not happened in lizards or other reptiles, although Howell (’36a, p. 305) believes the teres minor of mammals to be derived in this way.

3. By a posterior rotation of the scapulo-humeralis anterior., which process the writer believes to have been the mode of origin of the teres minor. 4. By an external development of the subscapularis, which

borders this region internally and, as noted above, may extend


around the lateral margin and on to the outer surface of the scapular blade.

The latissimus dorsi may be fused to some extent in lizards (as in urodeles) with the proximal end of the triceps. This appears to be a persistence of the embryonic connection between these muscles.

The lizard pectoralis has been considered by Rabl ('16, p. 685), following Mivart, to be an anterior continuation of the rectus abdominis. As me have seen, development offers no support to such a theory, based solely on adult topography.

Miner ('25, p. 217) believed that "the supracoracoid is not related to the pectoralis system, or to the coraco-brachialis"; the ontogeny, however, shows that such a relationship does exist, particularly with coraco-brachialis. Howell ( '36, p. 204) notes the interesting fact that the coraco-brachialis is sometimes innervated to a slight extent by N. supracoracoideus, the nerve proper to the supracoracoideus muscle. This presumably is due to variations in the cleavage of the primitive mass of pre-muscular tissue from which the two muscles are derived. Furbringer ('00, p. 418) states that in geckos and skinks the two muscles are intimately connected; this is presumably a retention of an embryonic condition, rather than a secondary fusion.

It has been suggested on the basis of a comparison of adult forms that the lacertilian type of two-bellied biceps has formed by a combination of elements differentiated proximally from coraco-brachialis, distally from brachialis (Romer, '22, p. 536 ; Howell, '36, pp. 204-205). This is in agreement with the ontogenetic picture.

The lizard shoulder girdle is notable for the presence of a varied series of fenestrae in the coracoid plate and the lower part of the scapular blade. These have sometimes been considered as structures formed independently of the musculature of the region, or as influencing the attachment of the muscles of this area. It is, however, much more probable that the reverse of this is the actual situation. It will be seen that the outlines of these fenestrae coincide with the areas of

DEVELOPMENT OF SHOULDER O F LACERTA 31

fleshy origin of scapulo-humeralis anterior and supracoracoideus, and often of the biceps as well. It thus appears probable that the fenestrae have developed as mechanisms allowing a “release” for the muscles concerned when they are contracted, just as the temporal fenestrae of reptiles have developed in connection with similar needs of the temporalis musculature and the thyroid or obturator fenestra of the pelvis is developed in relation to the origin of the obturator externus muscle, or its homologue. It is of interest that ontogenetically this area first appears as a solid plate and that the fenestrae develop secondarily, after the muscles are established.

Comparison with other reptile groups: Sphelzodofi. The new data acquired through the consideration of ontogentic processes may be applied to a comparison of lizard shoulder musculature with that of other reptilian groups. The development of the chelonian musculature is currently being studied in this laboratory by Mr. Warren Walker, Jr. and in consequence discussion of the Chelonia may be deferred.

The shoulder musculature of Sphenodon (best described by Furbringer, ’00, and more recently discussed by Romer, ’22 ; Miner, ’25 and Howell, ’35, among others) is generally recog- nized as quite similar to that of lizards. The writer once mistakenly assumed that lizards and Sphenodon are widely divergent forms which have inherited a common ancestral reptilian muscle pattern. However, it is now believed that lizards and Sphenodon are closely related, and hence simi- larities in musculature between the two may be due merely to specializations characteristic of this stock alone, and absent in primitive reptiles.

For the most part Sphenodon differs from the lizards in minor characters only. The lateral scapulo-humeral ligament is very prominently developed but separated from the scapular tendon of the triceps; the subscapular portion of the subcoraco-scapularis is relatively weak ; the scapulo-humeralis posterior (a portion of the latter muscle) is well developed on the outer surface of the scapula (a condition also true of


some lizards) ; the supracoracoideus tends to retain its embryonic intimate connection with the coraco-brachialis brevis.

The presence of a humero-radialis muscle is the one dis- tinctive feature of Sphenodon (firbringer, ’00, p. 495-500). This muscle is a weak lateral parallel to the triceps. At its origin it is intimately associated with the deltoid group; its insertion is by aponeuroses connected with the radial group of forearm muscles. It is innervated in part by the nerve supply- ing the deltoids, in part by a branch of the “radial” nerve. No such muscle is present in amphibians or turtles, but a rather comparable muscle is found in the Crocodilia. Since Sphenodon and the crocodiles are the only surviving diapsicls (although the two are but distantly related) it is reasonable to assume that the humero-radialis is a specialization developed by the diapsid reptiles. The lizards are presuiiiably derived from diapsid ancestors ; the absence of the muscle in them might well be deduced as a secondary loss.

Three modes of origin have been suggested for the huincro- radialis: (1) that it is a biceps derivative, (2) that it represents a longitudinal fusion of derivatives of deltoids and “supinator,” (3 ) that it is a laterally separated part of the triceps. None seems entirely satisfactory. The radically different innervation tends to rule out association with the biceps. While muscle fusions occur, close fusions are normallj- of a side-to-side type, and longitudinal fusions are usually readily discernible (as in the case of the reptile biceps).

It is to be hoped that eventually the ontogeny of one or the other of the two diapsid types may be investigated so that the mode of embryonic origin of humero-radialis may be tlis- covered. In the meantime, however, the lizard developmental story gives a significant clue as to the nature of this muscle. In stage I1 the deltoid mass is, we have seen, already distinct from the adjacent triceps. Distally, however, a band of tissue (h r? ; fig. 3) extends downward from the deltoid area along the lateral surface of the limb to the future elbow reyion. In stage I11 this band of tissue (hr? fig. 9) is still present, but has failed to differentiate toward a true muscular condition.


I n stage IV traces of this tissue band are still preqent, but it is regressive, and in stage V it has disappeared. Very probably this is the material which in Sphenodon develops into the humero-radialis. (I ts failure to develop in lizards is per- haps to be correlated with the lacertilian reduction of the radial nerve from which it gains its major innervation.) The humero-radialis thus appears to be associated with the deltoid group, which in diapsids tends to expand to an unusual degree down the lateral margin of the limb.

Crocodilia. The crocodilian shoulder 1iiuscles, well described in an early paper of Furbringer (1876), differ in a number of respects from those of lizards and Sphenodon; the general comparison, however, is obvious in most cases. The subcoraco-scapularis is scapular only in nature ; the scapulo- humeralis posterior is, as expected, closely associated with it. The humeral heads of the triceps are somewhat differently arranged and the coracoid head also attaches to a minor degree to the neighboring region of the scapula. The scapular deltoid is typically developed, but in the absence of a clavicle the clavicular deltoid homologue arises from the anterior margin of the scapula, and the scapulo-humeralis anterior is not differentiated from it. As noted earlier, a teres major has formed as a differentiation from the latissimus.

The Crocodilia, like Sphenodon, have a humero-radialis, which is here innervated exclusively by an “axillary” nerve and seems clearly to be a prolongation of the deltoid group, as Furbringer (’00, p. 517) believed. The ventral muscles show a number of variations, for the long portion of coraco- brachialis is absent, the biceps is (as in some lizards) tendinous rather than muscular proximally while the supracoracoideus, in contrast, is extensive and spreads upward on to the scapula. The crocodilians appear to exhibit merely a variation of the basic diapsid muscle plan, modified in relation to different functional needs and correlated with changes in skeletal structures.

Comparison with birds. It is highly desirable that the embryology of the bird pectoral musculature be investigated.


In the meantime, however, brief comments on avian homologies in the light of the present work may be justified. The discussion is based primarily on the excellent descriptions of Furbringer ( '02). Among the dorsal muscles, the triceps (anconaeus) and latissimus dorsi are comparable to their reptilian homologues, although the latissimus is subdivided and in the former the coracoid head is much reduced and but a single humeral head is developed. The deltoides propa- tagialis is a broad superficial muscle which arises from the clavicle and parallels the major deltoid muscle; it generally terminates, as a muscle belly, a t a point opposite the lateral process of the humerus, to which the deltoid major attaches. The muscle would thus appear to be a member of the deltoid group. However it does not attach to the lateral process, but is continued by a variable series of tendons to the wing, and in some cases the muscle belly extends well beyond the proces- sus lateralis. This suggests, as Furbringer observes, comparison with the humero-radialis, itself, associated with the deltoid group and presumably present in the birds' archosaur ancestors. Embryological data is needed. The powerful deltoides major and the small deltoides minor are certainly derived from the reptilian deltoid group, but a more detailed comparison seems inadvisable in default of knowledge of on t ogeny.

Apart from the deltoids, five muscles or muscle slips per- taining to the dorsal group arise from the inner surface of the girdle or scapular blade and attach to the proximal part of the humerus. For their proper determination embryological work will be necessary. Three of them, which attach in intimate association to the medial process of the humerus, are ascribed to the subcoraco-scapularis by Furbringer ; these include subscapular and subcoracoid elements and a slip from the lower part of the posterior margin of the scapular blade. It seems certain that the first two are correctly identified. The third is cornparable to certain of the variable muscle slips to which, as we have noted, the term scapulo-humeralis posterior (or profundus) has been applied. Since, however,

DEVELOPMENT O F SHOULDER O F LACERTA 35

this element in reptiles is clearly a derivative of the subcoraco- scapularis, no objection need be taken. The term scapulo- hunieralis posterior is used by Furbringer for a much larger muscle which arises broadly from the greater part of the scapular blade and converges downward to a humeral insertion. At first sight one is tempted to compare this with the reptilian scapular deltoid ; but, as Furbringer notes, it passes downward medial to the scapular triceps (rather than lateral to it) and inserts not with the deltoids but on the medial process. Further, because of its deep position it cannot well be a latissinius. derivative. The muscle thus appears to be definitely a member of the subcoraco-scapular group. The fifth (and last) of the muscle slips discussed is Furbringer’s scapulo-humeralis anterior, a small muscle arising from the lower part of the scapular shaft. Since it inserts well down the upper surface of the humerus rather than on the medial process, Furbringer’s interpretation is reasonable.

Of the ventral niuscles, the pectoralis is, of course, a large and complex structure in carinate birds but may be reasonably considered as elaborated from its simpler reptilian predeces- sor. The supracoracoideus is likewise enlarged as a muscle of flight (and extends on to the sternum at its origin) but is readily identifiable, and the biceps is comparable with its crocodilian homologue. The muscle termed brachialis inferior by Furbringer in birds is a small short muscle confined to the region of the elbow joint; its identity with the reptile muscle of the same name is doubtful. The coraco-brachiales of reptiles are represented in birds by two separate muscles, COSRCO-

brachialis externus (anterior) and interims (posterior). Both are short muscles and hence (as in the crocodiles representing the ancestral archosaur condition) there is no homologue of coraco-brachialis longus. The externus element is surely derived from the reptilian coraco-brachialis brevis. Coraco- brachialis internus is, in carinates, a large muscle which arises posterior to the supracoracoid muscle, from the lower end of the coracoid and the sternum and inserts on the humerus near its head. Furbringer regards it as a “Bildung sui generis”


and finds nothing comparable in lizards, Sphenodon and crocodiles. It is, however, even more closely Comparable to the typical coraco-brachialis brevis of reptiles than is the externus component of birds. The only possible objection is that it inserts on the medial process of the humerus, suggesting rela- tions to the subcoracoideus. Again, embryological data are needed.

Comparison with urodele dcvelopmeut . Of other vertebrate groups, shoulder muscle development has been studied, in a fashion similar to that here described for the lizard, only in the case of the urodele Necturus (Chen, ’35). This study was, a s Chen notes, suggested by the writer’s work on the pelvic region of the chick. The general nature of the developmental process is similar to that found by us in lizard limbs and the pelvic limb of birds. “The limb muscles in Necturus first arise as the dorsal and ventral premuscle masses. . . . From these premuscle masses the adult limb muscles a re gradually developed. . . . The embryological facts . . . add further support to the theory first advanced by Romer that the limb musculature of tetrapods originated from the two opposed muscle masses of the fish fin. ”(Chen, ’35; p. 42).

The phylogenetic position of urodeles is remote from that of lizards, and a comparison of the details of differentiation in the two cases should give evidence of importance regarding a number of muscular homologies which are in doubt. Part of the difficulties encountered a re due to the specialized nature of the urodele shoulder girdle, in which the dermal elements have been lost, while the primary girdle has developed a peculiar elongate anterior precoracoidal process. Other differences may be more basic in nature. Modern concepts of amphibian history indicate that the urodeles diverged from the line leading to reptiles at the very base of the tetrapod stem, and some writers even suggest an independent evolution from the fish stage. It is therefore possible that certain of the differences between urodele and reptilian muscle systems may be due to the two groups having undergone more or less


independent processes of differentiation from the simpler fish condition.

The adult condition of the xnusculature may be briefly noted. I n addition to excellent descriptions of urodele shoulder musculature by Fiirbringer (1873), Wilder (’12) and other authors, recent discussions on a comparative basis have been given by Miner (’25) and Howell (’35, ’36). A number of muscles are comparable with lacertilian homologues, including triceps (anconaeus) , latissimus dorsi, dorsalis scapulae (scapular deltoid) subcoraco-scapularis (scapulo-hurneralis, scapu- lohunieralis brevis, subscapularis) , supracoracoideus (coraco-humeralis), pectoralis, coraco-brachialis brevis, coraco- brachialis longus (glenoantibrachialis) and brachialis (brachialis inferior). There are certain differences even in these elements. The coracoid head of the triceps, as noted by Howell ( ’35, p. 421) passes medial to the ventral nerve trunk rather than by its usual more lateral route. The subcoraco-scapularis has no expansion on the inner surface of the girdle; but the adult urodele condition is comparable to that seen in the lizard in our stages I11 and IV. The major part of the supracoracoideus is comparable to that of reptiles, but there are addi- tional non-comparable portions discussed below. The coraco- brachialis brevis is much smaller than in lizards. The pectoralis lacks the anterior portion of the lacertilian muscle ; this is correlated with the absence of the interclavicle, from which the anterior portion of the lizard pectoralis arises.

Two regions are more difficult of comparison with the reptilian condition, those in which in reptiles the clavicular deltoid and biceps are situated.

A urodele cannot, a priori, possess a clavicular deltoid, since the clavicle is absent. In much the same position, however, we find the procoraco-humeralis longus (proscapulo-humeralis longus of Howell) which arises from the expanded “procoracoid” region. It passes backward to insert near the scapular deltoid, tends to fuse with that muscle, as does the reptilian clavicular deltoid, and like that muscle is innervated by a dorsal “axillary” nerve. The situation however is compli-


cated by the presence in this region of other smaller groups of fibers, some of which, lying beneath the procoraco-humeralis, are innervated by the supracoracoid nerve, while other shorter muscle slips with an “axillary ” innervation may be found beneath the main muscle or somewhat above it on the scapular region (deep slips of procoraco-humeralis, Miner ; proscapulo-humeralis brevis, Howell).

The urodele lacks a biceps of reptilian type ; some lack even a functional equivalent. I n others however, there is (as in anurans) a somewhat comparable structure, the coraco- radialis proprius. This includes a distal tendon which corre- sponds in position to the distal belly of the reptile biceps, and proximally a muscle arising, like the proximal belly of the biceps, froni the coracoid. But a tendon is hardly comparable to a muscle belly; the proximal muscular portion is intimately related to the supracoracoid muscle and innervated by the supracoracoid nerve, whereas the analogous reptilian muscle is associated with coraco-brachialis brevis and like that muscle is innervated by a typical ventral nerve branch.

The embryological picture gives a reasonable interpretation of the urodele musculature in comparison with that of lizards. Chen’s figures of an embryo of 17.5 mm. (his figs. 52, 53) are in general comparable to those given for stage I11 of our lizard descriptions. Here the embryonic dorsal group, as in lizards, includes latissimus, scapular deltoid and triceps ; the modest subcoraco-scapularis is not evident until somewhat later (27-mm. stage, fig. 58 sh).

Although for some reason Chen terms the procoraco- humeralis a ventral muscle, his figures show clearly (fig. 59, pch) that this muscle is an integral part of the dorsal mass and quite comparable in position to the clavicular deltoid of the lizard embryo (as seen in our stage IV). Chen does not mention the procoraco-humeralis brevis (proscapulo-humeralis brevis), but this muscle appears to be visible in his figure 52 as an outgrowth intermediate in position between scapular


deltoid (ds) and procoraco-humeralis (pch). It is immediately suggestive of the reptilian scapulo-hunieralis anterior, and this homology seems reasonable. More ventrally, there is at first a clear cut distinction between procoraco-humeralis and supracoracoideus (fig. 52). Slightly later, however (fig. 54) 19-mm. stage), the supracoracoideus is seen to have expanded upward so that it extends on to the base of the “procoracoid” beneath the procoraco-humeralis. Obviously, then, the presence of muscle slips on the “procoracoid” innervated by the supracoracoid nerve is a secondary condition.

The primitive ventral muscle mass includes, as expected, homologues of pectoralis, supracoracoideus, coraco-brachiales brevis and longus and brachialis. Necturus, unfortunately, lacks the coraco-radialis proprius and hence there is no evidence as to the mode of formation of this muscle. It seems clear, however, that its muscle belly must be derived from the prominent but undivided supracoracoid muscle present here. His figures are suggestive of the mode of origin of this muscle and of the reptilian type of biceps. I n figure 52 it will be noted that the supracoracoideus and brachialis * are closely opposed and jointly span the interval from coracoid plate to the lower leg. The detachment from the brachialis rudiment of mesenchyme to form a tendon, and the proximal association with this structure of a special portion of the supracoracoideus would result in the development of a coraco-radial muscle. In reptiles the more prominent coraco-brachialis brevis muscle occupies much of the area here covered by the supracoracoideus ; the biceps presumably arose through the association of a special portion of the coraco-brachialis with a muscle slip (rather than a tendon) derived from the brachialis.

Table of homologies. The homologies of the pectoral muscles for the groups discussed are presented in revised form in the accompanying table.

Labelled hm in erTOT.

ITR

OD

ELA

Lat

issi

mus

dor

si

Subc

orae

o-sc

apul

aris

IMto

ides

sca

pula

ris

Proc

orac

o-hu

mer

alis

lo

ngus

SP

RE

NO

DO

N

Lat

issi

mus

dor

si

Lat

issi

mus

dor

si

Lat

issi

mus

dor

si

Lat

issi

mus

dor

si

Subc

orac

o-sc

apul

aris

Su

bcor

aeo-

scap

ular

is

Sube

orac

o.se

apul

aris

Su

bcor

aco-

scap

ular

is

+ te

res

mai

or

(+

scap

ulo-

hum

eral

is

+ sc

apul

o-hu

mer

alis

+

scap

ulo-

hum

eral

is

k- po

ster

ior

post

erio

r)

post

erio

r po

ster

ior

F E

+ sca

pulo

-hum

eral

is

r

Del

toid

es s

capu

lari

s D

elto

ides

sca

pula

ris

Del

toid

es s

capu

lari

s U

elto

ides

tr

Del

toid

es c

lavi

cula

ris

Del

toid

es c

lavi

cula

ris

Del

toid

es c

lavi

cula

ris

m {

+ hu

mer

o-ra

dial

is

{ +

hum

cro-

radi

alis

tD

elto

ides

pro

pata

gial

is

@

maj

or +

mino

r

bd

LA

CE

RT

IIX

A

Proc

orac

o-hu

mer

alis

Tri

ceps

( h

neon

aeus

) br

evis

CR

OC

OD

ILIA

I

AV

ES

Scap

ulo-

hum

eral

is

Scap

ulo-

hum

eral

is

Par

t of

del

toid

ea

Scap

ula-

hum

cral

is

$ 0

ante

rior

an

teri

or

clav

icul

aris

an

teri

or

0

Tri

ceps

( A

ncon

aeus

) T

rice

ps (

Ane

onae

us)

Tri

ceps

(A

ncon

aeus

) T

rice

ps

(Anc

onae

us)

U

Cor

aeo-

brac

hial

is b

revi

s

Cor

aco-

brac

hial

is l

ongu

s B

rach

iali

s in

feri

or

Bic

eDs

Cor

aco-

bmch

iali

s br

evis

C

orac

o-br

achi

alis

bre

vis

Cor

aco-

brac

hial

is b

revi

s C

orac

o-br

achi

alis

ex

tern

us +

inter

nus

Cor

aco

brac

hial

is l

ongu

s C

orac

o-br

achi

alis

lon

gus

Abs

ent

Abs

ent

Bra

chia

lis

infe

rior

B

rach

iali

s in

feri

or

Bra

chia

lis

infe

rior

PB

rsch

iali

s in

feri

or

Bic

eDs

Bic

em

Bic

eos

Bic

eos

Pect

oral

is

I Pe

ctor

alis

I P

ecto

rali

s I P

ecto

rali

s I P

ecto

rali

s Ei

I Su

prac

orac

oide

us

s Su

nrac

orac

oide

us

I Su

prac

orac

oide

us

I Sup

raco

raco

ideu

s I

Supr

acor

acoi

deus


LITER,ATURE CITED

CIIEN, H. K. Derelopment of the pectoral limb of Necturus niaculosw. Illinois Biological Monographs, vol. 14, no. 1, 7 1 pp., 11 pls.

ERBRINQER, M. 1873 Zur vergleichenden Anatomie der Schultermuskeln. I. Theil. Jen. Zeitschr. f. Naturwiss. Bd. 7, S. 237-320, T. 14-18. 1874 Zur vergleichenden Anatomie der Schultermuskeln. 11. Theil. Jen. Zeitschr. f . Naturwiss., Bd. 8, S. 175-280, T. 5-7.

1876 Zur vergleichenden Anatomie der Schultermuskeln. 111. Theil. Morph. Jahrb., Bd. 1, 636-816, T. 23-27.

1900 Zur vergleichenden Anatomie des Brustschulterapparates und der Schultormuskeln. IV. Teil. Jen. Zeitschr. f . Naturwiss., Bd. 34, 8.

Zur vergleiehenden Anatomie des Brustscliulterapparateg und der Schultermuskeln. V. Teil. Vijgel. Jen. Zeitschr. f . Naturwiss., Bd.

HOWELL, A. B. 1933 Morphogenesis of the shoulder architecture. Par t I. Gen- eral considerations. Quart. Rev. Biol., vol. 8, pp. 247-259.

1933a Morphogenesis of the shoulder architecture. Par t 11. Pisces. Quart. Rev. Biol., vol. 8, pp. 434-456.

1935 Morphogencsis of the shoulder architecture. Par t 111. -4m- phibia. Quart. Rev. Biol., vol. 10, pp. 397-431.

1936 Morphogenesis of the shoulder architecture. Part IV. Reptilia. Quart. Rev. Biol., vol. 11, pp. 183-208.

1936a The phylogenetic arrangement of the muscular system. Anat. Rec., vol. 66, pp. 295-316.

MINER, R. W. The pectoral limb of Eryops and other primitive tetrapods. Bull. Am. Mus. Nat. Hist., vol. 51, pp. 145-312.

MOLLIER, 8. 1895 Die paarigen Extremitaten der Wirbeltiere. 11. Das Cieirop- terygium. Anat. Hefte, Bd. 5, S. 435-529, T. 31-38.

OSAWA, G. Beitrage aur Anatomie der Hatteria punctata. Arch. f . Mikrosk. Anat. u. Entw., Bd. 51, S. 481-691.

PERRIN, A. 1899 Contributions Q l’btude de la myologie cornparbe; membre anthrieur ches un certain nombre de batraciens et de sauriens. Bull. Sci. France et Belg., 32, 220-282, 2 pls. 1916 Muskeln und Nerven der ExtremitLten von Iguana tuberculata Gray. Anat. Hefte Bd. 53, S. 683-789, T. 18-22.

The locomotor apparatus of certain primi’ive and mammal- like reptiles. Bull. Am. Mus. Nat. Hist., vol. 46, pp. 517-606.

Pectoral limb musculature and shoulder-girdle structure in fish and tetrapods. Anat. Rec., vol. 27, pp. 119-143. 1942 The development of tetrapod limb musculature - the thigh of Lacerta. J. Morph., vol. 71, pp. 251-298.

WILDER, 11. H. 1912 The appendicular muscles of Necturus maeulosus. Zool. Jahrb. Suppl. 15, Bd. 2, S. 383-424, T. 23-27.

1935

215-718, T. 13-17. 1902

36, S. 289-736, T. 18-22.

1925

1898

RanL, C.

ROMER, A. S. 1922

1924

the development of tetrapod limb musculature — the shoulder region of lacerta

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