the development of tetrapod limb musculature — the thigh of lacerta

THE DEVELOPMENT O F TETRAPOD LIMB MUSCULATURE - THE THIGH O F LACERTA

ALFRED SHERWOOD ROMER The Biological Laboratories, Harvard University, Cambridge, Massachusetts

NINETEEN FIGURES

Perrin, in his useful paper of 1892 on pelvic limb muscles, commented on the fact that “si on ouvre un livre d’Anatomie comparee on est immediatement frappe du peu de developpe- ment don& & la myologie comparke.” With regard to limb musculature, this statement is nearly as true today as it was half a century ago; this despite numerous valuable recent contributions to this subject by Howell, Appleton, Haines and others. The homologies of the individual limb muscles of the various tetrapod classes is still in dispute in many cases, and generally accepted concepts of the grouping of limb muscles are still lacking.

In 1922 the writer pointed out that, since the musculature of the tetrapod limb had arisen phylogenetically from the two simple opposed dorsal and ventral muscle masses of the fish fin, it should be possible to classify tetrapod muscles into derived dorsal and ventral groups and thus establish a reasonable basis for an analysis of the complex situations encountered. This principle has been in some measure accepted by later writers, but numerous points of obscurity remain.

Much of this confusion is obviously due to the fact that for muscles, in contrast with other organ systems, the important evidence which might be derived from the developmental story was almost entirely lacking. Lack of embryological investigation appears to have been due to the general

251

252 ALFRED SHERWOOD ROMER

belief that little of value could be obtained from the early history of such plastic material as limb muscle tissues.

However, investigation of the development of the thigh musculature of the chick in 1927 showed, to the writer's surprise and pleasure, that the embryonic story of limb muscle differentiation could be made out with clarity in that form. The embryo at an early stage showed clearly the presence of two opposing masses of pre-muscular tissue, dorsal and ventral, from which developed, by a process of differentiation and splitting, the complicated muscle system of the adult. The embryological story showed a complete agreement in general and even in many details with the assumed phylogenetic process.

At that time a preliminary investigation was made of limb muscle differentiation in a number of other representatives of land vertebrates. This showed that similar processes of differentiation and cleavage of primary muscle masses could be observed in a variety of forms and that, therefore, it should be possible to establish satisfactory embryological criteria for the comparative study of limb muscles. Pressure of other duties, however, long prevented the writer from continuing these studies, and the work of Chen ('35) on the pectoral musculature of Necturus is the only investigation of this nature which has appeared in the intervening years.

The present work is concerned with the differentiation of the thigh musculature of Lacerta, as representative of the Lacertilia. The writer hopes to follow this with a description of the developmental processes of other portions of the limbs of Lacerta and of the limbs of a number of other land vertebrates in an effort to establish a comparative embryology for tetrapod limb muscles. The material used is from the Minot collection of the Harvard University Medical School, forming part of a series of sectioned embryos of Lacerta muralis collected at Naples, Italy. A considerable number of embryos was studied in preliminary fashion, and a few selected for detailed study and reconstruction by the wax plate method.

DEVELOPMENT O F THE THIGH O F LACERTA 253

The differentiation of limb musculature in Lacerta takes place rapidly. In several embryos with a crown-rump length of 5.0-5.2 mm. the limb buds are filled with a mass of seem- ingly indifferent mesenchyme in which it is difficult to dis- tinguish potential skeletal and muscular tissues, and even certain embryos with a length of 6.4 mm. are little further advanced. In contrast in an embryo of 9.0 mm. length differentiation is complete and essentially adult conditions obtain, and one individual of 7.6 mm. is nearly as mature. This is comparable to the situation in birds, in which the entire process occurs between the sixth and eighth days.

The muscle terminology used in the description of the lizard embryos is essentially the system of Gadow (1883), as used previously by the writer ( '32) for the adult lizards.

I am indebted to Drs. J. L. Bremer and G. R. Wislocki for the use of this material. The preliminary studies were aided by a grant from the research funds of the Division of Biology of the University of Chicago; completion of the paper was aided by a grant from the Milton fund of Harvard University.

DESCRIPTION

Stage I No attempt has been made in the present study to determine

the origin of the myogenic tissue (cf. the discussion by Chen, '35, pp. 11-15, 3940) ; Mollier (1895) claims that in Lacerta the premuscular cells are of myotomic origin. A first definite stage in differentiation is seen in embryo 815, with a crown- rump length of 6.4 mm. (certain, but not all, embryos of about 5.0 mm. are nearly as far advanced). The limb bud at this stage contains three layers of mesenchyme, arranged dorso-ventrally. The middle layer is that of the potential skeleton of girdle and limb ; above and below are longitudinal sheets of premuscular tissue, the future dorsal and ventral muscle masses. Their outlines are ill-defined, and there is little definite orientation of the cells. It is significant to note (with particular regard to the history of the caudi-femoral


muscles) that although the mesenchyme of these premuscular sheets approaches the myotomes closely at certain points (particularly postero-ventrally), it is not continuous with the myotomes, which are at this stage well-formed and with clear-cut outlines.

This stage is not illustrated here. Mollier (1895, pls. XXXV and XXXVI) has figured sections of Lacerta limbs at this stage, and the limb as seen in reconstruction is very similar to that which we have figured in the chick (Romer, '27, fig. 1).

Stage I I

Embryo no. 814, Minot Collection. Crown-rump length 6.4 mm. (figs. 1-5).

Skeleton. Girdle and limb are represented by a mass of condensed mesenchyme in which the shape of the adult structure is gradually appearing, but in which no separation between elements can be made out. I n the girdle, the acetabular region is present as a thick mass of pre-cartilaginous cells;

ABBREVIATIONS

Ac, acetabulum Adfem, adductor femoris Amb, ambiens Cf, caudi-femoral muscles Cfb, caudi-femoralis brevis Cfl, caudi-femoralis longus Cft, tendon of caudi-femoralis longus

running to knee region C1, cloaca1 muscle F, femur Fib, fibula Fmtb, femoro-tibialis Fte, flexor tibialis externus Fti, flexor tibialis internus (two parts) 11, ilium Ilfb, ilio-fibularis Ilfm, ilio-femora& Iltb, ilio-tibialis Is, ischium Istr, ischio-trochantericus Lig I1 Is, ilio-ischiadic ligament

Lig P Is, pubo-ischiadic ligament Nfem, femoral nerve N isv, ventral ischiadic nerve N obt, obturator nerve N per, peroneal nerve N tib, tibia1 nerve Oa, obliquus abdominis P, pubis Pife, pubo-ischio-femoralis externus Pifi, pubo-ischio-femoralis internus ( 3

Pit, pubo-ischio-tibialis ( 3 parts) Plp, processus lateralis pubis Pos, postsacral nerve ( 3 branches) Ps, presacral nerve (4 branches) Pt, pubo-tibialis R1, rectus abdominis lateralis S, sacral nerve Tib, tibia Trfm, triceps femoris Trp, transversus perinei

parts)

Ps III Pa II

POS I POS II POS III

Ftb

Fig.1 (left) Stage 11, skeleton and nerves of right pelvic limb in lateral

Fig. 2 (right) view. The digits are numbered.

Stage 11, skeleton and nerves in medial view.

Fig. 3 (left) Stage 11, the limb in lateral view. The dorsal muscle mass is shown, together with the anterior portion of the ventral mass. The general position of the future muscles is indicated.

Stage 11. As in figure 3, but the dorsal muscle mass has been removed and the limb diagrammatically sectioned a t the level of the future acetabulum, to show the ventral muscle mass from the deep surface next to the limb skeleton (cf. fig. 5) .

Fig.4 (right)

Fig.5 Stage 11. The limb in medial view, with the ventral muscle mass seen in surface view.

255


the ilium and distal parts of the pubis and ischium are formed of much thinner areas of mesenchyme with vague outlines. I n the pubis the obturator foramen has been formed, and a lateral projection indicates the site of the processus lateralis. The limb is short and the knee region is not identifiable except for the fact that at mid-length the shaft of the limb cleaves into presumed anlagen of tibia and fibula. The digits are indicated by buds of mesenchyme, two associated with the tibial portion, three with the fibular.

Nerves. Seven nerves take part in the formation of the limb plexus, including three which later prove to be presacral in position, the true sacral and two postsacrals ; the N. furcalis contributing to both lumbar and sacral plexus, is the second presacral. I n the lumbar plexus both obturator and femoral nerves are well formed. The former passes down through the obturator foramen to innervate the anterior proximal portion of the ventral muscle mass ; the latter passes outward over the anterior rim of the girdle to supply much of the proximal and anterior portion of the dorsal muscle mass.

Much more prominent is the sacral plexus, from which emerges a series of nerves showing the essential features of the adult pattern. Behind the base of the iliac blade a peroneal trunk runs outward to pass down the limb close to and slightly below the posterior margin of the dorsal muscle mass (the anlage of ilio-fibularis). At the presumed knee region this continues on down the extensor surface of the limb beneath the distal portion of the dorsal musculature. A second, larger trunk, the tibial nerve, lies at first close beside the peroneal, but turns more ventrally and splits into two portions which pass to tibial and fibular sides of the limb deep to the distal portion of the ventral muscle mass. Shorter branches include twigs to proximal portions of both dorsal and ventral groups, a peroneal nerve and a stem (N. ischiadicus ventralis) which passes downward medial to the future candi- femoral area to innervate the future flexor cruris group.

Muscles. As in stage I, dorsal and ventral muscle groups each consist of but a single mass of premuscular tissue. In

DEVELOPMENT OF THE THIGH O F LACERTA 257

each mass, however, differentiation has appeared to a considerable degree. The architecture of the dorsal mass is simple. It is relatively slender and elongate, the entire mass having its cells oriented in a proximo-distal direction. The proximal end is partially divided into two heads by the femoral nerve. The anterior head includes the anlagen of pubo-ischio- femoralis internus and ambiens ; the posterior head ilio- tibialis, ilio-femoralis and ilio-fibularis. More distally the areas anterior and posterior to the femoral nerve merge, but a second longitudinal fissure develops more posteriorly. This divides an anterior region, the future triceps, from the ilio- fibularis posterior to it. Still more distally at the presumed level of the knee, this fissure terminates, and the distal portion of the dorsal mass shows little evidence of differentiation.

The ventral musculature, although still a unit, is more complex in its topography. A proximal posterior portion, expanded anteriorly near the base of the limb and tapering posteriorly, obviously represents the future caudi-femoral muscles and presumably the flexor tibialis externus portion of the crural flexors. The posterior tip lies close to the proximal caudal myotomes, but is nevertheless quite distinct from them, a feature more clearly seen in embryo 812 (slightly more advanced). Seen from the ventral aspect the proximal portion of the ventral group extends far forward along the ventral edge of the girdle and down over the extremely short thigh region. The superficial portion of this region undoubtedly is the future flexor cruris, including flexor tibialis internus and pubo-ischio-tibialis. For the most part this sheet of tissue passes without break into the muscular tissue of the lower leg; anteriorly, however, a separate spur appears to be an incipient pubo-tibialis. A partially differentiated shorter internal portion of this ventral mass presumably includes anlagen of pubo-ischio-femoralis externus, adductor and ischio-trochantericus. The distal portion of the ventral mass divides into three spurs, representing radial and ulnar portions of the lower leg flexors and, centrally, the flexor digitorum communis.


Stage III Embryo 810. Crown-rump length 7.8 mm. (figs. 6-10). Skeleton. The skeletal elements are now in process of trans-

formation into typical cartilage ; the outlines of the girdle and major limb elements are well defined, and girdle, femur, tibia and fibula are clearly separable. The girdle is approaching its adult form; but both pubis and ischium are short, the

W Fig. 6 The limb in lateral view, showing dorsal surface of the

thigh. a, persistent connection of ilio-fibularis with peroneal muscles. Compare figure 2.

Stage 111.

lateral process of the pubis is short and stout rather than long and slender, and pubis and ischium are continuous below the thyroid fenestra. The limb bones are still very short.

Nerves. The nerve pattern is similar to that described above, but the nerve trunks are rather more elongated, and formed branches are more frequently discernible. The obturator nerve, as it passes down to the foramen, separates two portions of the pubo-ischio-femoralis internus and passes outward between adductor and pubo-tibialis. The femoral nerve


emerges onto the outer surface of the limb between ilio- tibialis and pubo-ischio-femoralis internus. I n the metazonal region the peroneal nerve passes downward above the caudi- femoral and beneath the ilio-fibularis to emerge on to the extensor surface anterior to the fibular insertion of the latter muscle. The tibia1 nerve likewise passes over the top of the caudi-femoral and then runs down the limb at a more ventral level; with increase in length of the thigh region, it has now

Fig. 7 Stage 111. As in figure 6, but ilio-tibialis, ilio-fibularis and ambiens have been cut to expose deeper muscles. a, strands of tissue still connecting pubo- ischio-f emoralis internus with the triceps group.

developed a trunk of moderate length before reaching a major bifurcation near the knee. There is a well developed N. ischiadicus ventralis running down medial to caudi-femoralis to branch out into the elements of the flexor cruris.

Muscles. Histological differentiation of muscular tissues is advancing at this stage, and, in gross morphology, the breaking up of the two muscle masses into the separate elements is far advanced. The muscle elements are, in cor- relation with the general proportions of the limb, short and

260 ALFRED SHERTVOOD ROMER

broad, and there are still various connections between the individual muscles. At the knee, the distal portions of both dorsal and ventral masses are nearly completely separated from the proximal portions, and we shall not here concern ourselves further with the distal musculature. A few connecting strands are still present, however.

In the dorsal muscle mass the ilio-fibularis, already partially separated in the last stage, is now completely separated from

Fig.8 Stage 111. Medial view, showing ventral surface of the thigh. a, cut head of part of gastrocnemius musculature. Compare figure 5.

the adjoining proximal elements. A small slip, however, still connects distally with the peroneal muscles. The ilio-femoralis has separated from the adjacent triceps. I n the triceps group, ilio-tibialis and ambiens together form a broad sheet of muscle extending from the formed tibia1 insertion up most of the length of the thigh; at the proximal end, separate iliac and pubic attachments are, however, present, separated by the pubo-ischio-femoralis internus, which passes over the margin of the girdle between them. The ilio-tibialis origin is less


extended than in later stages and is still single. Beneath the ilio-tibialis, separation of a distinct femoro-tibialis has begun. The pubo-ischio-femoralis internus is a single broad sheet of muscle arising from the upper surface of the pubis and inserting onto the upper surface of the femur. The muscle does not extend so far distally down the pubis or on to the inner surface of the girdle as it does later, nor is it divisible into

Fig. 9 Stage 111. As in figure 8, but the pubo-ischio-tibialis removed except a t its insertion, to show deeper musculature. a, tendinous area.

the several distinct portions seen in the adult. Distally, however, there is a beginning of the future subdivision of insertion areas. No trace was found of the slip which in the following stage reaches the femur ventral to the head of the ambiens. The muscle is still in process of separation from the triceps ; small strands still connect it with femoro-tibialis and ambiens.

I n the ventral muscle mass the complicated process of differentiation is well advanced. The tapering caudi-femoral musculature is more elongated posteriorly than in the last stage. Anteriorly it is for the most part separated from the


rest of the ventral musculature. The flexor tibialis externus appears to be in some regards a derivative of the caudi- femoralis, for it diverges outward and downward from the outer portion of the caudi-femoral muscle group to reach the knee region, where it is in contact with the lateral margin of the calf flexors. The ilio-ischiadic ligament, which forms a tendinous inscription across the base of the flexor externus (and part of caudi-femorales) in later stages, is as yet undeveloped. Somewhat farther anteriorly a small bundle of

n

Fig. 10 Stage 111. Lateral view, with all dorsal muscles and the limb skeleton removed, to show the ventral musculature from its deep surface. a, as in figure 9. b, slip passing from caudi-femorales to the posterior head of flexor tibialis internus. Compare figure 4.

fibers diverges from the caudi-femoral group to associate itself with the posterior belly of flexor tibialis internus. The entire caudi femoralis appears to insert on the ventral surface of the femur in a single area.

From the region of the future ischiadic tuber two stout muscle bellies arise, which represent the flexor tibialis internus. The posterior one is, as noted, still partially connected with the caudi-femorales. Distally it is still in contact


with the flexor musculature of the calf. The more anterior belly 6f flexor tibialis internus is united in its fleshy insertion with pubo-ischio-tibialis (gracilis). Although in figure 9 the flexor tibialis internus is shown as discrete with the removal of the overlying “gracilis” sheet, both bellies are actually intimately bound with the pubo-ischio-tibialis for much of their length.

The last named muscle forms a broad sheet covering most of the flexor aspect of the thigh. Posteriorly there is retained, as in the adult, a line of contact with flexor tibialis externus. Proximally the muscle has little contact with the girdle; the pubo-ischiadic ligament, from which much of the muscle arises in the adult, is almost undeveloped, although a mass of mesenchyme connecting the muscle with the postero-ventral angle of the ischium appears to represent the beginning of this ligament. The muscle is partially subdivided proximally into two portions, a thick posterior head (Pit. 111) covering the flexor tibialis internus, and a thinner anterior head (Pit. 1-11) which fails to extend, as does that of the adult, up the external surface of the pubis.

That anterior and internal portion of the ventral mass which was partially distinct in the last stage is now far advanced in the process of cleavage into pubo-tibialis, adductor femoris, and pubo-ischio-tibialis externus (fig. 10). The pubo-tibialis is completely separated from its neighbors, and its distal end has swung back deep to the other flexors to insert near the knee joint toward the fibular margin of the articular area. Adductor femoris and pubo-isehio-femoralis externus together form a stout mass of tissue lying beneath the proximal part of the femur and external to the pubo- ischium. Distally the mass separates into a proximally inserting portion, the pubo-ischio-femoralis externus, and a more distal adductor.

The one muscle whose status is uncertain at this stage is the ischio-trochantericus. As may be seen in figures 14 and 17, this small element in the adult passes from the ischium to the head of the femur, located, so to speak, in the notch between


the antero-dorsal margin of the caudi-femorales and the postero-dorsal edge of the pubo-ischio-femoralis externus. The muscle is certainly a derivative of the ventral group and must be, at this stage, included in either the caudi-femoral mass or the pubo-ischio-femoralis externus. The general position of the muscle suggests a derivation from the caudi- femoral mas's, as is the case in the chick (Romer, '27).

S tage IT7

Embryo 1602. Crown-rump length 9 mm. (figs. 11-19).

Skeleton and Zigarnenfs. Girdle and femur are well formed in typical cartilage, with much the shape seen in the adult. The processus lateralis pubis is prominent. An unchondrified gap is present between the lower ends of pubis and ischiurn, in contrast to the complete lower boundary of the thyroid fenestra seen in the last stage. There is a long hypoischiadic extension of the girdle ventro-posteriorly. The internal trochanter near the head of the femur is u7ell developed. A small accessory cartilage lies between the head of the femur and the fibula. Joint ligaments (not figured) are already well developed.

Of great importance for muscular attachments are the strong ligaments which curve around the under side of the limb as it emerges from the trunk; they are here, as in the adult, well developed. The ilio-ischiadic ligament connects the lower margin of the iliac blade with the angular tuber ischii. It runs downward over the caudi-femoralis longus, expands into a triangular form, and then turns forward to its ischiadic attachment. Many of the fibers of the caudi-femoralis attach to the upper portion of the ligament, which runs inward as a tendinous inscription to interrupt the continuous course of the caudi-femoral mass. From the ligament arises the flexor tibialis externus; indeed, it is probable that a portion of the fibers caudad to the ligament may be considered as belonging properly to this muscle. The more posterior portion of the flexor tibialis internus arises near the point of insertion of

DEVELOPMENT O F THE T H I G H O F LACERTA 265

the ligament into the ischium. From the ventral margin of the ligament certain axial muscles take origin, the transversus perineus and a cloaca1 muscle.

The pubo-ischiadic ligament completes the ventral liga- mentous arch. I t s anterior extremity is attached to the processus lateralis pubis. Thence it runs posteriorly with a

Fig. 11 Stage IV. The pelvic girdle in lateral view. The ilio-ischiadic and pubo-ischiadic ligaments are indicated (the ilio-pubic ligament is not well developed a t this stage).

convex lower margin, across the outer surface of the pubo- ischium, superficial to pubo-ischio-femoralis externus, to attach to the posterior margin of the ischium near the attachment of the ilio-ischiadic ligament. From it arise the anterior portion of the flexor tibialis internus, the pubo-ischio-tibialis and the adductor femoris, and in addition certain elements of the trunk musculature.

I n the adult the ligament series along the base of the limb is completed by an ilio-pubic ligament bridging over the pubo- ischio-femoralis internus. This, however, is little developed in the embryonic material.


Nerves. The lumbar plexus is, as before, formed by the N. furcalis and the two preceding nerves, and forms two main trunks. The more anterior gives off a branch supplying the lower (pubic) portions of the pubo-ischio femoralis internus and passes downward between two divisions of that muscle through the obturator foramen as the obturator nerve. Emerg- ing from the foramen, it supplies much of the pubo-ischio- femoralis externus and passes outward between the two portions of that muscle. After giving off a branch to the adductor

Fig. 12 Stage IV. The thigh in lateral view, showing the dorsal musculature. Compare figures 3 and 6 .

femoris, it passes outward dorsal to that muscle and to the pubo-ischiadic ligament to terminate in branches to pubo- tibialis and pubo-ischio-tibialis.

The femoral nerve, second of the lumbar trunks, passes outward beneath the front edge of the ilium, overlying the

'This twig is, essentially, merely one from the general lumbar plexus, and should not lead to the statement sometimes made that the pnbo-ischio-femoralis internus is in part supplied by the obturator nerve.

DEVELOPMENT O F THE THIGH OF LACERTA 267

most posterior part of the pubo-ischio-femoralis internus, which it supplies. The main trunk passes distally along the anterior border of the ilio-tibialis, superficial to the pubo- ischio-femoralis internus, and terminates in cutaneous branches. Short branches innervate all the various portions of the triceps femoris and the ilio-femoralis.

Fig. 13 Stage IV. As in figure 12, but ilio-tibialis, ambiens, pubo-tibialis and pubo-ischio-tibialis have been removed. This figure is comparable in most regards with figure 7.

The ischiadic plexus is formed by the furcalis and the three next posterior roots, which converge downward internal to the ilium; plexus formation occurs in the region posterior to the acetabulum, beneath ilio-femoralis and ilio-fibularis and along the anterior margin of the caudi-femoralis. Short proximal branches pass to the ilio-femoralis and, piercing that muscle, to the ilio-tibialis, to ilio-fibularis, and, more ventrally, to ischio-trochantericus, adductor femoris and pnbo-ischio- femoralis internus. The main trunks leaving the plexus are


three in number. Two pass outward dorsal to the caudi-femoral muscles, N. peronaeus and N. tibialis. Neither gives branches of importance to the thigh musculature ; they proceed directly to the lower leg. The former passes down between ilio- femoralis and ilio-fibularis, lies close to the inner margin of the latter muscle in the distal portion of the thigh, and crosses over the distal tendon of that muscle to reach the

Fib

i N

Fig. 14 Stage IV. Median view, showing part of the ventral surface of the thigh. Compare figures 5 and 8.

fibular margin of the lower leg. The tibia1 nerve is more deeply placed, and is ventral rather than posterior in position. It passes down the thigh close to the lower surface of the femur, parallel to the long caudi-femoral tendon, and sheathed ventrally by the middle portion of the crural flexor group.

The element passing ventral to the coccygeo-femoralis muscles is the N. ischiadicus ventralis of Frets ('10, p. 90) and Appleton ( '25, p. 372). This appears to contain a small cutaneous component (not shown in the figures) but mainly


functions as a nerve supply to much of the flexor cruris musculature. It is short, and just above the point at which the ilio-ischiadic ligament attaches to the ischium, divides into a number of branches which enter flexor tibialis internus, flexor tibialis externus, and the posterior portion of pubo- ischio-tibialis.

Fig. 15 Stage IV. Ventral view, the mid-line of the body a t the top. I n order to demonstrate more clearly the proximal portion of the ventral musculature, the thigh has been diagrammatically shifted to extend laterally.

This scheme of innervation is in general agreement with that found in other lizards.

Musculature. The condition of the musculature at this stage is essentially that found in the adult animal ; except for minor details the present embryo agrees perfectly with typical lacertilian conditions. The elongation of the limbs has enabled the muscles to elongate to adult proportions. With the development of the ilio-ischiadic and pubo-ischiadic ligaments, the proximal attachments of the thigh muscles are of adult type, and in various cases the tendinous type of insertion


characteristic of the adult has replaced the vague and fleshy attachments earlier present. The individual muscles are in as discrete a condition as is ever attained; connections between proximal and distal limb segments have entirely disappeared (except for one persistent flexor tendon retained in the adult). The situation pictured here is highly comparable to that figured, for example, by Perrin (1892, pl. 23) in Uromastix.

Fig. 16 Stage IV. As in figure 15, but with the pubo-ischio-tibialis removed to expose the deeper members of the flexor series.

Of the dorsal muscles, the ilio-fibularis has changed little except for elongation and loss of the slight connection with the distal musculature noted in the last stage, and ilio- femoralis is likewise little changed. In the triceps group, ilio- tibialis and ambiens are distinct for a considerable portion of their length; ilio-tibialis is divided into two p’ortions at its head (the anterior head muscular, the posterior tendinous) and the posterior margin has grown to cover much of the ilio-fibularis. The femoro-tibialis is greatly expanded. Pubo-

DEVELOPMENT OF T H E THIGH O F LACERTA 271

ischio-femoralis internus has spread broadly over the dorsal surface of the pubis and the interior of the girdle, has divided into several portions and has developed a series of discrete areas of femoral insertion ; former connections with the triceps have entirely disappeared.

Ventrally, too, further differentiation has taken place. The caudi-femorales form a complex group. Posteriorly the muscle extends back along the tail for about eight segments, and has

N tib-

Fig.17 Stage IT. Lateral view of the thigh, with dorsal muscles and limb elements removed, to show the deep surface of the ventral muscles. Compare figures 4 and 10.

secondarily .become intimately associated with the adjacent caudal axial musculature. Anteriorly the muscle is completely divided longitudinally into two components, caudi- femoralis longus and caudi-femoral; s brevis. The muscle is partially divided traiisversely beneath the ilium by a tendinous inscription which is continuous with, and a portion of the ilio- ischiadic ligament. This ligament has appeared since the last

2’72 ALFRED SHERWOOD ROMER

stage described, and the inscription, hence, is probably not of primary importance in the history of this muscle group. At the femoral end, three areas of attachment are now developed. Two adjacent areas are situated ventro-posteriorly for caudi-femoralis brevis and the greater part of caudi-femoralis longus; a stout tendon from the latter, however, curves forward beneath the bone to a more anterior attachment. From

Lig,ll I n

Fig. 18 Stage IT. Lateral view, with the limb sectioned about one-third way down the femur. Axial muscles attached to the ilio-ischiadic and pubo-ischiadic ligament are included here.

a point close to its femoral attachment a long slender tendon passes from caudi-femoralis longus down to the knee region, close to the tibia1 nerve and adjacent to the posterior belly of flexor tibialis internus. This tendon was undeveloped in the last stage described; there, however, it was noted that a connection existed in this area between the caudi-femoral mass and the posterior belly of flexor tibialis internus. Pre- sumably this characteristic reptilian tendon has arisen by a


“pulling off ” of this connection, the tendon forming from connective tissue associated with the flexor tibialis internus. Association of tendon and flexor tibialis internus tends to be confirmed by the fact that in certain lizards (Gadow, 1882, p. 400) the caudi-femoralis tendon and flexor tibialis are still in contact in the adult.

Still relatively undifferentiated, as in the adult stage of all lizards, is the massive group of thigh flexors including flexor tibialis externus, flexor tibialis internus and pubo-ischio- tibialis. These muscles are partially separated proximally

N

Pit I

Fig. 19 Stage IV. Left, section of the thigh half way down the femur, looking proximally. Compare figure 18. Right, section through the thigh close to the distal end of the femur, looking toward the knee joint, t o show the insertions of the flexor muscles.

and in great measure separated at their insertions ; for most of their course, however, they form a closely connected mass of musculature. Externally the posterior ‘portion of this group, which may be termed as a whole the flexor cruris, is described as the flexor tibialis externus; the greater portion is a sheet showing little superficial evidence of subdivision, which is customarily termed the pubo-ischio-tibialis, o r gracilis. Internal to the middle portion of the gracilis are two partially discrete bellies termed by most writers flexor tibialis internus. The relations of these elements at different levels are best seen in the sections shown in figures 18 and 19. Proximally the origins of these muscles lie in a continuous

2 74 ALFRED SHERWOOD ROMER

series along the course of the ilio-ischiadic and pubo-iscliiadic ligaments. The origin of the flexor tibialis externus lies most posteriorly and dorsally, and it seems reasonable to assume from the embryological situation seen in the last stage that part of the fibers included in the caudi-femorales posterior to the inscription represent a cut-off portion of flexor tibialis externus (cf. Appleton, '28, pp. 416418). Next anterior in position, along the lower portion of the ilio-ischiadic ligament, is a thick posterior portion of pubo-ischio-tibialis (Pit. 111) which was already partly differentiated in the last stage. From this point forward a thin sheet of pubo-ischio-tibialis (Pit. 11) lies along much of the length of the pubo-ischiadic ligament ; anteriorly, close to the pubic end of the ligament, is a second thicker and partially discrete portion of pubo-ischio-tibialis (Pit. I). Near the point of attachment of the two ligaments to the ischium, the two heads of flexor tibialis internus arise internal to the middle portion of pubo-ischio-tibialis and continuous with it. This essential continuity of the flexor cruris mass is a persistent expression of the common embryological origin of the muscles concerned.

Distally, however, the various areas of attachment are sharply defined. As the writer and other authors have noted the attachments tend to segregate into two groups, one anterior (or medial) to the gastrocnemius, the other more toward the fibular side of the limb between the two heads of that muscle. The anterior area of insertion, toward the medial side of the tibia, is a fleshy one in our specimen, and is utilized by the entire pubo-ischio-tibialis and the anterior head of flexor tibialis internus (Fti. I). The posterior or lateral area is utilized by tendons from flexor tibialis externus and the posterior head of flexor tibialis internus (and by the pubo-tibialis and long caudi-femoral tendon as well). A reminder of early continuity of the ventral musculature is the persistence of an additional tendon from flexor tibialis externus which joins the lateral head of the gastrocnemius ; the earlier association of flexor tibialis internus with the distal flexor musculature has however, disappeared.


Pubo-tibialis has persisted with little change except elongation, running from the processus lateralis pubis diagonally outward and backward beneath the flexor cruris to insert with the posterior group of tendons. Proximally there is some adherence between this muscle and adjacent fibers of pubo-ischio-femoralis externus (not shown in the figures), but not to the degree seen in the adult. The adductor femoris and pubo-ischio-femoralis externus are well differentiated. The former arises from the pubo-ischiadic ligament deep to pubo- ischio-tibialis and inserts along a line running far down the ventral surface of the femur. The latter arises fleshily from almost the entire external area of pubo-ischium and the thyroid fenestra; its femoral insertion is divided into two portions, one into the ventral intertrochanteric fossa, the second more anteriorly on to the developed internal trochanter. Ischio- trochantericus is now developed, taking origin from the inner posterior surface of the ischium and emerging above the tuber ischii to insert on the femur near its head.

As regards innervation, the muscles derived from the dorsal mass receive a nerve supply as follows : pubo-ischio-femoralis internus, ambiens and femoro-tibialis are innervated entirely from the crural plexus (all except the first from the femoral nerve). Ilio-fibularis is supplied only by the ischiadic plexus. Ilio-tibialis and ilio-femoralis, however, are doubly innervated, with twigs from both crural and ischiadic plexus. The primitive dorsal mass was doubly innervated; in the process of differentiation the more anterior and posterior components have been restricted to a supply from the most nearly adjacent source; however, the process of cleavage has not strictly followed the line of division between the two sources, and the double innervation of the last two muscles named is due to a persistence of an earlier embryonic (and presumably phylogenetic) condition of the dorsal mass.

Similar conditions are seen in the derivatives of the ventral muscle mass, which primitively was innervated anteriorly by the obturator nerve from the crural plexus and posteriorly

276 ALFRED SHEBWOOD ROMER

by metazonal ischiadic derivatives. Of the shorter muscles, with a femoral attachment, the caudi-femorales and ischio- trochantericus, placed far posteriorly, are innervated solely from the ischiadic plexus. Pubo-ischio-femoralis externus and adductor femoris,2 however, appear to be doubly innervated by ischiadic and crural derivatives.

Of the longer muscles, the pubo-tibialis, which we have seen to have been, in early stages, placed far anteriorly, has a purely crural innervation. The great crural flexor mass, however, receives nerves from both prozonal and metazonal sources. The flexor tibialis externus, placed far posteriorly, is exclusively ischiadic in innervation. Flexor tibialis internus in most lizards (including Lacerta) is also ischiadic; but in many reptiles (as first noted by Gadow, 1882, p. 401) a twig from the obturator nerve reaches this muscle. Pubo-ischio- tibialis is always doubly innervated by obturator and sacral components, as would be expected from its great antero- posterior extent.

DISCUSSION

General cornsideration of deuelogme.ntn1 history. As indicated in the preceding description, the differentiation of the pelvic limb musculature of Lacerta is a well-ordered process. There are first established two primary masses, dorsal (extensor) and ventral (flexor), lying on opposite sides of the developing limb skeleton. The first major stage in differentiation is a division of both masses at the knee region into proximal and distal portions (the latter are not further considered here). Somewhat overlapping this process, but for the most part subsequent to it, occurs the differentiation of individual muscles in the proximal segments of both dorsal and ventral masses. This process of cleavage may be dia- gramatically represented as follows :

a Despite Gadow’s statement (1882, p. 407) to the contrary.

DEVELOPMENT O F T H E THIGH O F LACERTA 977

Dorsal muscle mass

Posterior dorsal muscles

Anterior dorsal muscles

Flexor group

Ventral muscle mass

Caudal group

Deep group

Ilio-fibularis Ilio-f emoralis Ilio-tibialis

Femoro-tibialis Ambiens Pubo-ischio-femoralis internus

Pubo-ischio-tibialis Flexor tibialis internus Flexor tibialis externus

Caudi-f emoralis longus Caudi-femoralis brevis Ischio-tr ochantericus

Pubo-ischio-femoralis externus Adductor femoris Pubo-tibialis

There is no a priori reason to assume that the processes of differentiation seen in Lacerta have any relation to the phylogenetic history of the musculature concerned. One might, for example, assume that the various groupings seen among the developing muscles are purely fortuitous, merely a “practical” method of sorting out an undifferentiated mass of premuscular tissue into the definite adult muscles. Numer- ous considerations, however, indicate that this is not the case, and that the pattern of differentiation seen in the embryo is a conservative one, reminiscent of the phylogenetic history of the tetrapod limb in its evolution from the fin. Most con- vincing in this regard is the nature of the primary division of the musculature into dorsal and ventral masses, each extending far antero-posteriorly and each innervated by both prozonal and metazonal nerves. No strong argument can be


made for the interpretation of this situation on the grounds of developmental “convenience. ’ ’ In the adult, it is true that there is at the distal end of the thigh a functional division into dorsal extensor muscles and distal flexors, but proximally the musculature forms a complete sheath with a variety of functional uses for the varied components. One might more reasonably expect, on embryological grounds, that if a major cleavage were to occur, it would be into anterior and posterior rather than dorsal and ventral groups. Nerves and muscles are closely associated in development; one might expect a primary division of the premuscular tissue into anterior and posterior masses associated respectively with the prozonal and metazonal nerves.

The division actually present agrees, however, with the probable phylogenetic history of limb muscles. The writer in 1922 pointed out that the tetrapod limb has been derived from that of a fish fin in which the relatively simple musculature was arranged in opposed dorsal and ventral masses, and that the muscles of adult tetrapods could be classified into two groups which were presumably derived from these two ancestral masses. This thesis, now generally accepted, was proposed without the support of embryological work. It is, however, in almost perfect agreement with such developmental data as is available. In the case of the chick (Romer, ’27) the developing musculature is first present as a pair of masses, dorsal and ventral, whose derivatives are, with certain reasonable corrections, the muscles assumed on phylogenetic grounds to have been derived from the historically ancestral dorsal and ventral muscles of the fish fin. This situation is found in the limb of Lacerta as well.

Again, many of the features of cleavage of the two primary groups are more readily interpreted on a phylogenetic basis than on a purely embryological one. Particularly interesting in this regard is the fact that cleavage in many cases does not coincide with the division between areas of innervation, as one might expect on functional grounds. In Lacerta, for example, two of six dorsal muscles of the adult thigh region


have double innervations ; of nine named ventral muscles, three are doubly innervated.

In the writer's original classification of reptilian muscles ('22, pp. 596-597) the presumed dorsal muscles were the triceps, ilio-fibularis, pubo-ischio-femoralis internus and ischio-trochantericus; presumed ventral components were pubo-ischio-tibialis, pubo-tibialis, flexor tibialis internus, flexor tibialis externus, adductor femoris, and pubo-ischio- femoralis externus ; the caudi-femorales were left incertae sedis. The study of chick embryology indicated that this interpretation was for the most part correct, but that two modifications were necessary : the ischio-trochantericus is a ventral muscle, not a dorsal one, and the caudi-femoral muscles are integral components of the ventral limb series. The present work shows an exactly similar situation in the lizard. Here again the caudi-femorales are definitely derivatives of the ventral limb muscle mass, and, although there is uncertainty as to the exact mode of origin of ischio-trochantericus, it is unquestionably part of the ventral series.

The primary object of the present work is to afford an embryological basis for the comparison of the thigh musculature of the lizards, as presumably typical reptiles, with that of other classes of tetrapods. Since, however, comparable studies have not yet been made in amphibians and mammals we will confine our discussion to a comparison with the embryological situation seen in the bird and to a consideration of the reptilian thigh region in the light of lacertilian embryology.

Comparison with chick. If the processes of differentiation seen in the thigh of Lacerta be compared with those previously described for the chick (Romer, '27), it appears that the development is very similar in the two cases. By reference to the tabular summary of differentiation on page 371 in connection with the table of suggested homologies on page 378 of the work cited, it is seen that the muscles derived from the two primary muscle masses are identical in the two cases.


Beyond this primary division, however, differences appear in various regards. These differences are apparently due to three factors. (1) The adult pelvic structure differs radically, and hence the topography of the two forms necessarily differs during development. (2) The adult components are not identical; elements present in one form may be absent or fused with adjacent muscles in the other. (3) The “timing” of cleavage of muscle groups may differ somewhat and thus give apparent differences in muscle relations although the end result may be the same. Thus, for example, given three muscles A, B and C derived from a common “matrix,” A might divide from the other two slightly before C separates from its relatives or vice versa without any implications of radical difference in the homologies concerned.

In the dorsal group a feature of difference lies in the fact that in Lacerta a first division proximally is that between a posterior group including ilio-fibularis, ilio-tibialis and ilio- femoralis on the one hand, from ambiens and pubo-ischio- femoralis internus on the other, whereas in the chick the first cleavage is between deep and superficial portions. This, however, appears to be but a slight difference in “timing” in the two cases, and ilio-fibularis and the components of the triceps femoris group are readily homologized (despite the avian development of a pseudo-sartorius) .

More difficult (Romer, ’27, pp. 374-375) is the determina- tion of the homologues of lizard ilio-f emoralis and pubo-ischio- femoralis internus among the series of short muscles which run dorsally from girdle to femur in the chick. These include (1) a posteriorly placed ilio-femoralis externus, (2) two stout ilio-trochanterici, (3) an ilio-femoralis internus, much more anterior and ventral in position. The first is obviously allied with the reptilian ilio-femoralis ; the last surely comparable with part, at least, of pubo-ischio-femoralis internus ; the ilio-trochanterici are of doubtful homology. Comparison of reptilian development with that previously described for the chick suggests that the ilio-trochanterici are derived from an expanded ilio-femoralis and that in the chick the ilio-


femoralis internus is the lone survivor of the pubo-ischio- femoralis internus. We have noted that in the lizard this last muscle separates a t an early stage from ilio-femoralis, but that a connection long persists between it and the anterior part of the triceps, particularly the ambiens ; the pubo-ischio- femoralis internus can in a sense be pictured as a proximal offshoot of the ambiens. In the chick the ilio-femoralis internus appears fully formed in “Stage 111” (Romer, ’27, fig. 32). It is far removed in general position from the other dorsal femoral muscles. The writer assumed that it had been derived from the deep dorsal mass shown in figure 2 of that paper. This, however, would necessitate a very rapid differentiation coupled with a rapid shift in position. On the other hand, the area of the triceps labeled “Ambiens” in figure 2 includes the area in which ilio-femoralis internus is later seen, while the Ambiens in “Stage 111” is restricted to a more distal position. Hence the avian ilio-femoralis internus, like the reptilian pubo-ischio-femoralis internus, is probably differentiated from the antero-proximal portion of a primitive triceps mass. Pubo-ischio-femoralis internus and ilio-f emoralis internus are, therefore, probable homologues, while the ilio- trochanterici are derived from the reptilian ilio-femoralis as their development and position posterior to the femoral nerve would suggest.

I n lizard and chick the development of the ventral mass proceeds along essentially similar lines. The process of differentiation here is a complex one. The ventral mass has to arrange itself into an essentially triangular pattern, with tail, hip region and knee as the three apices of the triangle.

From tail to femur are the pair of caudi-femoral muscles, clearly identifiable as homologues in the two cases, although the avian muscles (termed coccygeo-femorales) are naturally shorter and less powerful. I n the lizard we have noted that it is highly probable that the ischio-trochantericus is a derivative of the caudi-femoral group, but that its differentiation was not seen in the material studied. In the chick, however,


the homologous ischio-femoralis is clearly seen to separate from the coccygeo-femoral group.

Of the ventral muscles running longitudinally outward from the pelvis along the limb both lizard and bird possess two short elements attaching to the femur; quite certainly the reptilian pubo-ischio-femoralis externus = avian obturator, reptilian adductor = avian pubo-ischio-f emoralis. In both cases the two muscles concerned are in contact in early stages ; marked differences in their position at later stages are cor- related with marked differences in construction of the pubo- ischium.

In reptiles the pubo-tibialis arises from a portion of the ventral mass in common with the last two muscles. No homologue of pubo-tibialis is discernible in either embryonic or adult fowl. Three hypotheses are possible : (1) the muscle was present in avian ancestors but has been lost. (2) The muscle had not been differentiated in the reptiles from which birds have been d e r i ~ e d . ~ (3) Since the pubo-ischio-femoralis is double in the fowl, possibly one of the two represents a pubo-tibialis which has shortened so that it attaches to the femur rather than to tibia (or fibula). In the case of the second and third of these alternatives the pubo-tibialis would be represented in some fashion by a portion of the adjacent and embryologically related pubo-ischio-f emoralis ; and even under the first alternative this might also be the case.

With the marked change in pelvic construction in birds has been associated a great change in the architecture of the crural flexor group. In the fowl this includes a caud-ilio-flexorius from tail and ilium, an ischio-flexorius, and an accessorius originating from the femur and joining the ischio-flexorius. The caud-ilio-flexorius is posteriorly placed and long retains a connection with the coccygeo-femoralis longus ; its homology with the flexor tibialis externus seems assured. The ischio- flexorius, the only other major component, is innervated solely by the ischiadic plexus, and the insertion is by a tendon as-

Birds are archosaur descendants, and the crocodiles, the only surviving archosaurs, lack this muscle.

DEVELOPMENT OF THE THIGH OF LACERTA 283

sociated with the gastrocnemius. No part of the flexor mass is innervated by the obturator nerve; no portion of it inserts on the tibia medial to the gastrocnemius. This implies that the pubo-ischio-tibialis and anterior portion of flexor tibialis internus, both prominent in the embryo as in the adult lizard, have disappeared in birds. No trace of these muscles is seen in the bird embryo. The ischio-flexorius is apparently equivalent to the posterior head of flexor tibialis internus in reptiles. It will be noted that the crocodile shows an inter- mediate condition (Romer, '23, pl. 22, fig. 2) . Here a portion of the flexor cruris group still attaches to the medial side of the tibia ; but the pubo-ischio-tibialis is already much reduced.

A characteristic feature in both lizards and crocodiles is the possession of a tendon passing down from caudi-femoralis longus to the knee region. It has been noted that in the lizard embryo this tendon seems to have evolved from a persistent connection between caudi-femoralis longus and the posterior head of flexor tibialis internus (= ischio-flexorius). In birds an accessorius flexor arises from the femur distal to the insertion of coccygeo-femoralis longus and attaches to the ischio-flexorius. This muscle is generally believed to be associated phylogenetically in some manner with the reptilian tendon. The embryological studies discussed here shed no light, however, upon this matter, for there is no evidence that the accessorius is connected at any stage with the coccygeo- femorales. The writer believed the accessorius to be an up- growth from the gastrocnemius. The evidence for this, however, is slight, and Appleton's suggestion ('28, pp. 426427) that it represents a caenotelic femoral attachment of part of the flexor mass is quite possibly correct.

Howell has upon two occasions ( '38 a, '41) compared avian and lacertilian limb muscles. In general his homologies appear to be the same as those in the writer's earlier paper and those given here, although his use of unusual terminologies for both reptile and bird makes for some uncertainty.

The ilio-trochantericus anterior is considered by him to be a derivative of pubo-ischio-femoralis internus ; as we have


noted the embryology indicates that it is, rather, derived from ilio-femoralis, as is the closely associated posterior ilio- trochanteric muscle. Howell terms the anterior ilio-trochantericus the iliacus, stating that “thire appears to be no doubt of its homology” with the mammalian muscle of that name, since it is found “arising from a situation comparable to that in many mammals.” Such a positive identification, however, seems rash in view of the fact that mammals and birds have arisen independently from reptiles in which no separate iliacus is present and in which there is no anterior expansion of the ilium to serve as a potential iliacus area of origin. Howell homologizes with the reptilian adductor femoris (a muscle of modest size) both adductors of the bird and in addition the obturator muscle ; while the avian ischio- femoralis is assumed to include not only the obviously homologous ischio-trochantericus of reptiles but also the equivalent of the massive pubo-ischio-femoralis externus of reptiles. This assignment of the last named muscle is improbable on any grounds and is contradictory to the embryological evidence.

Thigh musculature ifi adult lizards. The embryological story sheds considerable light on the architecture of the lacertilian thigh and the interrelations of the component muscles. Earlier work on this topic, including the important papers of Gadow (1882), Perrin (1892) and Rabl ( ’16) was considered by the writer in 1922; since that time several authors have made contributions which may be briefly discussed.

Appleton ( ’28) concerned himself only with the post-axial portion of the lizard thigh musculature, particularly the flexors, in connection with a discussion of the homologies of these muscles throughout the tetrapods. Of particular importance is his demonstration of the fact that nerves from the ischiadic plexus which innervate the thigh muscles follow

He states that this muscle “has uniformly been mistaken” for the mammalian obturator internus. This, however, is not the case; compare, for example, Romer, ’27, p. 378; bird obturator = mammal obturator externus; mammal obturator internus = bird ischio-femoralis.


two distinct paths, the first (followed by the main nerve trunks to the lower leg) passing above the caudi-femoral muscles, the second (N. ischiadicus ventralis) passing below these muscles. This topographic division is used by him as a major feature in establishment of muscle homologies.

Haines (’34, ’35, ’35a) has discussed the evolution of the flexor muscles of the tetrapod thigh in a series of papers notable for their .author’s scepticism regarding the phylogenetic constancy of nerve supply. His descriptions of lacertilian musculature are brief but clear and accurate and are illustrated with simple but useful figures.

The discussion of lacertilian limb myology by Ribbing (’38) in the recent “Handbuch der vergleichenden Anatomie” is based upon the literature and contributes little except the unfortunate addition of still another series of new and un- familiar terms for the thigh muscles ; the ilio-fibularis alone escapes the dubious honor of a change of name.

Howell (’38) treats briefly of lizard muscles in a general essay on the evolution of tetrapod thigh muscles ; his account lacks clarity because of the use of a nomenclature at variance in many regards with that used by any other writer; this nomenclature is not explained in the text and the illustrations are inadequate. Two muscles are listed for “Iguana” under the term pubo-tibialis. Of these, the pubo-tibialis anterior appears to be the muscle universally called the ambiens. His pubo-tibialis medius is in the position of a true pubo-tibialis, but was said to have a femoral innervation, whereas the pubo- tibialis is always innervated by the obturator. This error appears to be associated with the fact that the correctly labeled obturator nerve of his figure 3A is called femoral in figure 3B ; in another paper (’41, p. 285) he reports that the muscle “in a later specimen proved to have only ventral (i.e., obturator) innervation.” The term pubo-ischio-fernoralis, usually applied to the reptilian adductor femoris, is used twice for muscles which appear to be the pubo-ischio-femoralis

5Data from Doctor Howell indicates that the form used is not Iguana but a related genus.

286 ALFRED SHERT1700D ROMER

internus and pubo-ischio-femoralis externus. The ilio- femoralis is stated to be innervated only from the peroneal; however, Gadow (1882, p. 387), Rabl ( '16, p. 741), the writer, and Haines ( '35, p. 357) all find a femoral innervation as well.

I n connection with the innervation of muscles, Howell dis- cusses the evolution of the pelvic girdle as related to nerve stems. Several modifications of his account may be suggested. He believes ('38, pp. 182, 187) that the obturator nerve at first emerged on to the limb by passing over the dorsal margin of the pubis, and only later adopted a course through the obturator foramen. This may have been the case, but if so the shift must have been at a very early piscine stage, for the obturator foramen is already well developed in the old Carboni- ferous amphibians. Galechirus, which he uses (fig. 1R) as an example of a stage antecedent to the use of the obturator foramen in reptiles is actually a mammal-like reptile in which the obturator foramen has not only appeared but is well advanced in its development toward the mammalian type of obturator fenestra. The pelvis termed Iguana (fig. 1C) is in reality that of the pelycosaur Ophiacodon (Williston, '16, p. 229, fig. 77, reversed).

Howell in his treatment of pelvic limb musculature ('36, '38, '41) has tended to set up four muscle groups in the limb. He has, of course, made a division between dorsal and ventral groups, following the phylogenetic history, but has tended to place as great or greater emphasis on a vertical cleavage between muscles supplied by anterior nerves (femoral, obturator) and those supplied by metazonal trunks. In a series of studies in comparative myology carried out some two decades ago under Dr. TV. K. Gregory by a group of students including C. L. Camp, J. P. Chapin, G. K. Noble and the writer, this same fourfold classification was at first adopted. It was, however, soon abandoned, for it became obvious that division of dorsal and ventral groups into anterior and posterior components was artificial and rested on no adequate phylogenetic basis. The present study and that on the chick show that such division is equally artificial from an embryological point

DEVELOPMENT O F T H E THIGH OF LACERTA 287

of view. A fourfold division may be of some “practical” use in pigeon-holing muscles in mammals, where double innervations are rare, but cannot well be used for lower tetrapods and must be recognized as entirely artificial in nature.

In lizards the components of the dorsal muscle group are in general clear-cut, discrete elements - ilio-fibularis, ilio- f emoralis, the triceps group (including ilio-tibialis, ambiens, and f emoro-tibialis) and pubo-ischio-femoralis externus. Pos- teriorly they are clearly marked off from any members of the ventral group, although ventral flexor components may ascend to the ilium via the ilio-ischiadic ligament. Anteriorly the pubo-ischio-femoralis internus may approach or gain contact with adjacent ventral muscles (pubo-ischio-femoralis externus, pubo-tibialis), but the embryology indicates that such conditions are secondary.

Of interest are the intimate relations shown embryologically between pubo-ischio-femoralis internus and the adjacent portions of the triceps (ambiens, femoro-tibialis). A priori one would believe the first named muscle to be more closely associated with the other dorsal muscles from girdle to femur - the ilio-femoralis -than with a set of muscles extending beyond the knee joint. But we have noted that one of the first indications of cleavage of the dorsal mass is the separation proximally of an anterior slip which appears to include pubo- ischio-femoralis internus and in addition the proximal portion of the ambiens and perhaps femoro-tibialis. Even in the embryo figured as stage I11 traces of connections between pubo-ischio-femoralis internus and these triceps components persist. It may perhaps be significant that in urodeles (cf., for example, Perrin, 1892, pl. 17) the area in which the ambiens and femoro-tibialis are found in reptiles is there occupied by pubo-ischio-femoralis internus.

The ventral thigh group, presumably in relation to its more important functions in support and progression, is more complex and difficult of analysis. lJTe believe that, following the embryological picture, it may be interpreted as including (1) a group of muscles directed anteriorly to insert on the


femur (coccygeo-femorales, ischio-trochantericrs) ; (2) a deep group extending from the girdle outward along the limb (pubo- ischio-femoralis externus, adductor femoralis, pubo-tibialis) ; and (3) a superficial ventral flexor sheet or flexor cruris (including pubo-ischio-tibialis, flexor tibialis internus, flexor tibialis externus).

Because the caudi-femoral muscles take origin not from the girdle but from the tail and run forward in close contact with the axial muscles, they are frequently regarded as “extrinsic” muscles which do not properly belong to the appendicular musculature ; thus, for example, Howell ( ’38, p. 192) classifies them as “axial muscles to the thigh.” The developmental history of these muscles shows definitely that this is not the case. In the chick (Romer, ’27, fig. 2a etc.) the coccygeo-femoralis is an integral part of the ventral muscle mass and even when first beginning its differentiation is completely separated from the axial musculature. The situation seen in Lacerta is as strong in proof of its appendicular nature. The caudi-femoral mass in early stages is definitely a component of the ventral mass.

The mesenchyme from which the caudi-femorales arise lies close to the myotomes, but is distinct from them and continuous with the remainder of the pre-muscular tissue of the limb ; the close apposition of caudi-femoralis longus and the axial musculature of the tail seen in the late embryo and adult is secondary. The caudi-femorales are fundamentally as “intrinsic” to the appendage as any other limb muscles; it is merely their misfortune (so to speak) that their function demands an origin from the tail rather than from the girdle.

As noted earlier, the embryological origin of the ischio- trochantericus is not clear in the Lacerta material studied, but it appears to be a slip detached from the margin of the coccygeo-femorales (as is definitely the case in the chick). In Lacerta the ischium is short and the developed muscle (fig. 14) runs at a marked angle to the parent mass. I n primitive reptiles, however (cf. for example, Romer, ’22, pl. 14, figs. 3, 5) the ischium is elongated posteriorly, with its dorsal margin

DEVELOPNENT O F THE THIGH O F LACERTA 289

obviously close to and paralleling the course of the caudi- femorales. I n such forms an ischio-trochantericus could arise simply by adherence of ventral caudi-femoral fibers to the bone directly adjacent.

I n stage I1 of our description there is already becoming evident a thickened proximal deep portion of the ventral muscle mass, centering in the region between pubis and femur. From this develop pubo-ischio-femoralis externus and, more superficially, adductor femoris. The two are apparently closely related muscles, and their differentiation is slow and still incomplete a t our stage 111. With these two muscles (rather than with the flexor cruris group) appears to be associated the pubo-tibialis, despite its tibia1 insertion. The pubo-tibialis is already distinct distally from the typical crural flexors at stage 11, and at no later stage has it the slightest connection with these muscles. I ts “area of origin” in stage I1 would appear to be from the same deep anterior mass of tissue from which pubo-ischio-f emoralis externus and adductor femoris arise. In later stages and in the adult the pubo-tibialis lies close beside these muscles and runs parallel to them. We may be justified in considering the three muscles as forming in theory (and probably phylogenetically) a conical mass of tissue extending from the girdle out beneath the limb, with pubo-ischio-femoralis externus, adductor femoralis and pubo-tibialis representing functional divisions based on their successively more distal points of insertion. It is of interest to note that in such a urodele as Salamandra (Perrin, 1892, pl. 17, fig. 14) there are no muscles closely comparable to adductor femoralis or to pubo-tibialis but instead a single muscle partaking of features of both, combining the area of insertion of the former with the area of origin of the latter.

Haines (’34, pp. 23, 25, 27) states that the use of pubo- tibialis is confused and proposes to replace that term by flexor intercapitis anterior as regards the muscle here termed pubo-tibialis, while a muscle which he terms “Gadow’s pubo- tibialis” is named adductor tibialis. With this I cannot agree. Gadow’s pubo-tibialis (1882, p. 409) is, in Sphenodon and in


most lizards, a single muscle with an obturator innervation which runs diagonally across the flexor aspect from the pubic tubercle or its neighborhood deep to the general flexor cruris group. Only in varanids (“Hydrosaurus”) does Gadow men- tion a “part I” which is, on the contrary, a dorsal muscle with a femoral innervation which appears to be a subdivision of the ambiens, as is a similar crocodilian muscle. It is this last muscle which Haines terms “ Gadow’s pubo-tibialis,” but it appears to have been only a minor element in Gadow’s concept of pubo-tibialis.

There remains for consideration the great superficial sheet of ventral flexors running to the knee region, to which, following Gadow, we have applied the names pubo-ischio-tibialis (‘ ‘ gracilis ’ ’) , flexor tibialis internus and flexor tibialis externus. These are not three discrete muscles but, as has been seen, are fused to a considerable degree and vary even within the Lacertilia as regards the nature of their components. Appleton (’28) has suggested that this complex be termed the flexor cruris. Apparently he proposed to include under this name only that portion of the flexor mass considered in his work (confined to the metazonally innervated muscles) ; it is here adopted in a broader sense to include also the more anterior portions of pubo-ischio-tibialis (and flexor tibialis internus) which have an obturator innervation. It must be emphasized that the pubo-tibialis, although functionally related to the flexor cruris group, is (as has been seen) ana- t omically distinct.

The interrelations of the various components of the lacertilian flexor cruris group are best seen in the sections of figures 18 and 19. Their areas of origin lie superficial to those of the other thigh muscles over a broad band along the ventral and posterior margins of the limb bone from lateral pubic process to ischiadic tuber to ilium via the intervening ligaments. Near their origins all the components are adherent to one another.


Distally there is a segregation into two areas of origin, as emphasized particularly by Haines ( ' 3 5 ) .

Haines justly complains of the rather unnatural nature of the Gadow nomenclature and proposes to resolve the difficulty by renaming the muscles concerned. We do not see, however, that any great advantage is gained by this, other than an addition to the existing plethora of terms, and have adhered, as before, conservatively to the Gadow system, using roman numerals as suffixes where necessary. The equivalents of Haines' terms are as follows :

Flexor cruris

USAGE HERE HAINES Pubo-ischio-tibialis I Adductor tibialis Pubo-ischio-tibialis I1 Pubo-ischio-tibialis Pubo-ischio-tibialis I11 Flexor tibialis inferior Flexor tibialis internns T Flexor tibialis internus I1 Flexor tibialis externus

Flexor intercapitis posterior Flexor tibialis genicularis Flexor tibialis externus

Appleton ('28, fig. 13, etc.) lays considerable stress on the distinction between dorsal and ventral heads of the flexor cruris mass as important in phylogeny. However, as Howell ('38) notes, this distinction is perhaps not too fundamental. I n lizards, as we have seen, ilium and ischium are connected by the ilio-ischiadic ligament, and flexors may take origin at any point along it. I n the absence of the ligament, the flexors will naturally be separated into dorsal (iliac) and ventral (pubo-ischiadic) portions ; but there is no guarantee that the line of separation is always the same.

Sphenodon. It is improbable that material for the study of thigh development in this reptile will become available to the writer ; it seems reasonable, however, to believe that developmental processes in this surviving rhynchocephalian are similar to those in lizards, since the general muscular arrangement is very similar. Gadow (1882), Perrin (1895), Osawa (1598) and Frets ('10) have published on the Sphenodon thigh, and the writer's own dissections agree with their descriptions.


There are few points of contrast with the general lacertilian condition. There are differences in details of subdivisions and attachments of pubo-ischio-femoralis internus and pubo- ischio-femoralis externus. I n relation, apparently, to the poor development of the iliac blade, the ilio-ischiadic ligament is undeveloped dorsally, the ilio-fibularis arises from the verte- bral column behind the ilium rather than from that element, and the "flexor tibialis externus" is more intimately connected with the caudi-femoral muscle mass. This last feature is essentially a retention of the embryonic conditions of our stage 111.

Marked differences are found, however, in the flexor cruris group. Instead of the well-defined lacertilian subdivisions, there is a nearly continuous sheet extending around the ventral and posterior aspects of the thigh. The more anterior portion inserts medially on to the tibia, and presumably may be compared with pubo-ischio-tibialis and flexor tibialis internus I of lizards. The posterior superficial portion and an incompletely separable deep mass may be compared with flexor tibialis externus and flexor tibialis internus 11, since they insert more laterally beneath the knee joint and since the presumed flexor tibialis externus has the characteristic tendon to the lower leg. It seems obvious that the flexor cruris mass begins its development in Sphenodon, as in lizards, as an undifferentiated sheet, and that in the former there is less differentiation of discrete muscle bellies in the adult.

Crocodilia. The thigh musculature of the alligator was described by the writer in 1923 and compared with that of the Lacertilia. Appleton ('28, p. 414) notes an error in my statement that the posterior head of the adductor has a partial ischiadic innervation. Howell ('38, p. 209) fails to find a partial obturator innervation in the flexor tibialis internus which has been reported by Gadow (1882, p. 401), the writer ( '23, p. 540) and Haines ( '34, p. 31 ; '35 a, fig. 4, flexor tibialis gcnicularis) .

Haines ( '34, '35 a ) confirms the writer's description and in general agrees with his comparisons. With regard to the

DEVELOPMENT O F T H E T H I G H O F LACERTA 293

CROCODILE (ROMER, ’23)

Pubo-ischio-tibialis Flexor tibialis internus I Flexor tibialis internus I1 Flexor tibialis internus Flexor tibialis internus I V Flexor tibialis externus

flexor series, however, he suggests a different interpretation in two instances. The differences are set forth in the following table of flexor homologies, using the writer’s nomenclature rather than that of Haines :

LIZARD HOMOLOQUES LIZARD HOMOLOQUES (ROMER, ‘22) (HAINES. ’34, ’35 a)

Pubo-isehio-tibialis Pubo-ischio-tibialis I1 Flexor tibialis internus I (pt) Flexor tibialis internus I Flexor tibialis internus I (pt) Pubo-isehio-tibialis 111

Flexor tibialis internus I1 (pt) Flexor tibialis internus I1 Flexor tibialis externus

IIIFlexor tibialis internus I1 (pt) Pubo-tibialis

Flexor tibialis externus

The differences have to do with the two mu,scle slips termed by the writer parts I1 and I11 of flexor tibialis internus in the crocodiles. We believe that Haines is correct in considering the first of these comparable with the posterior portion of the pubo-ischio-tibialis of lizards. That the lizard pubo-tibialis, however, is equivalent to flexor tibialis internus I11 of the crocodilians is extremely unlikely. The two have nothing in common except that they are laterally inserting flexors. The pubo-tibialis has an obturator innervation. the crocodilian muscle an ischiadic one. Haines believes this un- important; but such a flagrant breach of the “proprieties” could only be justified if the rest of the evidence tended to confirm the homology, which is not the case. The origins of the two muscles are in strong contrast. The pubo-tibialis arises from the pubis, the supposed crocodilian homologue is attached to the posterior edge of the ischium. To get from the one point to the other phylogenetically the supposed pubo- tibialis would have had to migrate over a long and circuitous route and “by-pass” several other members of the ventral flexor series.

Haines further suggests that the muscle which other writers have considered an accessory head of the ambiens in crocodilians is the same muscle as the anterior portion of the pubo-ischio-tibialis in lizards (his adductor tibialis ; Pit. I of the present paper). This also appears improbable. The


lacertilian muscle inserts with the rest of the pubo-ischio- tibialis in a flexor position on the inner side of the tibia, whereas the supposed crocodilian homologue is an integral part of the triceps femoris; the lizard muscle is innervated by the obturator nerve, the crocodile muscle by the femoral. ,It is to be hoped that the development of the crocodile thigh will be investigated at some future time; the embryological evidence should be decisive, since it is assignment to primitive dorsal or ventral groups that is at stake.

Primitive reptilian thigh musculature. In his work of 1922 the writer attempted to deduce the nature of the thigh muscles of the ancestral reptiles by studying the musculature of lizards and Sphenodon in conjunction with the skeletal material of the oldest known fossil forms. One source of possible error not then realized must be pointed out.

It was then generally believed that Sphenodon and the lizards were phylogenetically far removed from one another, the former being a diapsid, the latter belonging to a different subclass, the Parapsida. I n consequence it was assumed that muscular features common to the two types must be considered as inherited from the " stem reptiles. " Sphenodon and the lizards are very similar myologically and it was hence assumed that both had retained much of a primitive reptile muscle pattern.

It is now, however, strongly suspected that the Squamata are of diapsid derivation and that Sphenodon and the lizards are hence actually closely related. In consequence muscular similarities between the two mean relatively little in terms of general reptile phylogeny. We must seek a wider basis of comparison in order to deduce conditions in a primitive reptile. Available evidence, however, can be gained from but two other sources, the Crocodilia and the Chelonia. These are none too satisfactory, for both are obviously specialized and the former order, technically diapsid, may also belong to the same general group as the Rhynchocephalia and Squamata.

Such evidence as these groups give, however, tends to confirm the picture of general reptilian conditions deduced from

DEVELOPMENT OF THE THIGH OF LACERTA 295

the study of the lizards and Sphenodon, for many of the muscles found in these forms are present in little modified condition in crocodilians and turtles.

It would seem probable that the components of the dorsal muscle group in the ancestral reptiles were essentially those seen in lizards and Sphenodon today, including ilio-fibularis, ilio-femoralis, pubo-ischio-f emoralis and the three typical triceps members ; presumably, however, the ilio-tibialis had but a single head and the pubo-ischio-femoralis internus may have been less complex in nature.

I n the ventral group there was undoubtedly a powerful caudi-femoral muscle mass inserting on the femur, although one cannot be sure of its subdivisions. Both embryological and comparative evidence suggest that the ventral part of the caudi-femoral mass was partially adherent to the flexor cruris group. Ischio-trochantericus and pubo-ischio-femoralis externus were presumably similar to the condition seen in lizards and there was undoubtedly an adductor femoris. The pubo-tibialis is, however, known only in lizards and Sphenodon and it is far from certain that such a muscle was differentiated in early reptiles; more probably it was present as part of a more inclusive adductor extending to the knee region.

The flexor cruris was undoubtedly present as a broad sheet of muscle covering the ventral and posterior surfaces of the thigh. Presumably there was already some functional subdivision of this sheet into bellies, and distally the medial head of the gastrocnemius, we may assume, must have caused a separation of the tibia1 insertions into two groups, as in modern forms. However, it is unlikely that the six components commonly found in the modern lizards were present as such; Sphenodon is probably closer to the original condition in its flexors.

Below is presented a table of thigh muscle homologies between the groups discussed here. The nomenclature for lizards and Sphenodon is that used in the present and earlier papers by the writer; the crocodilian terminology is that of Romer ( '23) ; avian muscles as in Romer ( '27).


Ilio-fibularis ~ Ilio-fibularis

Ilio-fernoralis 1 Ilio-fernoralis

LACERTILIA 1 SPHENODON I CRaBeDfLIA I AVES

Ilio-fibularis

Ilio-f emoralis

Triceps femoris: ilio-tibialis

Pubo-ischio- f emoralis internus

1

Pubo-ischio- Pubo-ischio- 1 Ilio-fernoralis f emoralis f emoralis internus internus

Ambiens

Femoro-tibialis

Pubo-ischio- tibialis I

Pubo-ischio- tibialis I1

Pubo-ischio- tibialis I11 ,

D O R S A L G R O U P

ilio-tibialis ilio-tibialis

Ambiens Ambiens I + I1

Femoro-tibialis Femoro- tibialis

I

Pubo-ischio- tibialis

Triceps femoris :

+ sartorius '

Ambiens

Femoro-tibialis

ilio-tibialis

Flexor tibialis internus I

Flexor tibialis

Flexor tibialis Flexor tibialis internus internus I

Flexor tibialis

I I

I

Pubo-tibialis

Adductor femoris

Pubo-ischio- f emoralis externus

Ischio trochantericus

Ilio-fibularis

Pubo-ischio Adductor femoris f emoralis Pubo-tibialis

Adductor femoris

Pubo-ischio- Pubo-ischio Obturator f emoralis f emoralis externus externus externus

~

Ischio- Ischio- Ischio- trochantericus trochantericus femoralis

Ilio-f emoralis externus +

Ilio-trochantericus

brevis + longus ~~

I Flexor cruris: 1 I 1 ............

Pubo-ischio- tibialis

Flexor tibialis internus I1

............

............

. . . . . . . . . . . .

. . . . . . . . . . Ilio-flexorius

Caud-ilio-flexorius

Coccygeo- f emorales

DEVELOPMENT O F T H E THIGH O F LACERTA 297

LITERATURE CITED

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GADOW, H.

GREGORY, pi. K., AND C. L. CAMP 1918

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Some muscular changes in the tail and thigh of reptiles and

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