Homology and Evolution of the Deep Dorsal Thigh Musculature in Birds

Home , Evolution of birds, Homology (biology)

JOURNAL OF MORPHOLOGY 189327-346 (1986)

Homology and Evolution of the Deep Dorsal Thigh Musculature in Birds and Other Reptilia TIMOTHY ROWE Department of Geological Sciences, University of Texas, Austin, Texas 78713

ABSTRACT Data from adult birds, crocodilians, Sphenodon, squamates, turtles, and from the chick embryo are compared to test conflicting hypotheses of homology of the deep dorsal thigh muscles of birds and other reptiles. This comparison suggests that: 1)avian Mm. iliofemoralis externus and iliotrochantericus caudalis (herein renamed “iliofemoralis cranialis”) are homologous with M. iliofemoralis of other reptiles; 2) avian Mm. iliotrochanterici cranialis and medius are homologous with one of two divisions of M. pubo-ischio-femoralis internus found in other reptiles (pars dorsalis of Crocodylia); 3) avian M. iliofemoralis internus (herein renamed “cuppedicus”) is homologous with the other division of M. pubo-ischio-femoralis internus (pars medialis of Crocody- lia). This hypothesis implies a minimum of seven transformations in the number of muscles and their positions of origin and insertion in the evolution of Aves, five of which are recapitulated during ontogeny of the chick. The traditional recognition of three muscles in the “iliotrochantericus group” is topographically accurate, but it is a misnomer and has been a source of misdirection when these muscles are studied in a phylagenetic context. Varia- tions within Aves in the presence of the iliotrochantericus muscles (cranialis or medius) and the iliofemoralis muscles (externus or cranialis) are results of heterochronic perturbations of a conserved developmental program. Unlike most previous interpretations, this view of homology suggests that the evolution of avian bipedality was accompanied by few myological transformations, despite profound modification of the skeleton.

The homologies of the deep dorsal thigh complex, involving possible loss of primitive muscles of birds with those of other amniotes muscles, evolution of new muscles, reappear- have been among the most problematic in ance of lost muscles, fusion of muscles, and avian myology (George and Berger, ’66; Van- changes in their innervation and action. den Berge, ’79). This is in part a reflection of However, disagreement exists on precisely the large transformation that occurred in the which of these transformations are most hip. Avian evolution involved a shift from likely to have occurred. This controversy is the quadrupedal locomotion of primitive ar- further manifested in disagreement on the chosaurs to the bipedal stance of birds, dur- identity and distribution of some of these ing which the skeleton of the pelvis and muscles within Aves. The problem is compli- hindlimb were transformed until even the cated by a nomenclature in which a large most primitive living birds are markedly dif- number of names has been applied with ferent from other living reptiles. Conflicting varying usage to a much smaller number of opinions on these homologies occur in the anatomical structures (Table 1). literature, reflecting different opinions on One source of conflict is that different anat- avian phylogeny and, more fundamentally, omists have chosen different amniote taxa different criteria used to test homology. From for their comparisons with birds, and they these accounts (Gadow, 1880, 1882; Gadow disagree on which taxon is most informative and Selenka, 1891; Romer, ’23a, ’27a,b, ’42; in studying avian history. Supporting evi- Walker, ’77; Lance Jones, ’79), historic transformation of the avian deep dorsal thigh Timothy Rowe is now at the Department of Geological Sci- musculature appears to have been extremely ences, University of Texas, Austin, TX 78713. 328 T. ROWE dence for most of the various hypotheses of homology has come from Crocodylia and Squamata, with the latter usually being considered the more informative of the two groups. Romer ('23a), for example, compared birds with crocodilians but reached only an admittedly tentative conclusion regarding the homologies of avian deep thigh muscles in non-avian amniotes. He was unable to re- solve his uncertainty even after studying development of the thigh muscles of the chick, finding that "the embryological evidence is. . . inconclusive" (Romer, '27a, p. 375). Later, however, after studying development of the thigh in the squamate Lacerta, Romer changed his opinion without reservation to favor a different view of the avian homologies, citing what he considered to be conclu- sive evidence (Romer, '42). Walker ('77) agreed at length with Romer's second opinion and promoted additional corroborative arguments based on squamate characters. Others have chosen to compare birds either with adult mammals (Howell, '38), or with mammalian ontogenetic stages (Lance Jones, '79). rn Compelling evidence has long existed that ."e Aves shares a more recent common ancestry with Crocodylia than with any other living taxon, that Squamata is a more distant relative, and that Chelonia and Mammalia are even more remotely related (Fig. 1; e.g., Gaff- ney, '80; Gauthier, '84; Gauthier et al., in press). Consequently, estimates of the relevance of squamate characters to this issue may be mistaken, because any homologous characters shared by Aves and Squamata could have evolved no more recently than in their most recent common ancestor, i.e., the most recent common ancestor of Sauria (sensu Gauthier, '84: Sphenodon + Squa- mata + Crocodylia + Aves). Hence, comparisons of birds with squamates or mammals are informative with respect to the more distant history of birds, but not on the evolution of archosaurian or uniquely avian characters. In this study I reexamine the homology of deep thigh muscles in birds by employing the hypothesis that Aves and Crocodylia are sister groups comprising Archosauria, and that Lepidosauria, Chelonia, and Mammalia are its consecutively more distant outgroups (Fig. 1). I also examine the development and distribution of deep thigh muscles within Aves. This comparison supports a different hypothesis of avian thigh muscle homology from that currently accepted by most students. EVOLUTION OF AVIAN DEEP THIGH MUSCLES 329

3- P

LEPIDOSAURIA ARCHOSAURIA Y SAURIA

REPTlLlA

AMNIOTA I

Fig. 1. Phylogeny of higher systematic categories of Amniota employed in this study (from Gauthier, '84; Gauthier et al., in press).

Phylogeny of the avian deep dorsal thigh tory and University of California (Berkeley) musculature appears to be far less complex Museum of Paleontology were also exam- than generally believed, and despite many ined, to confirm positions of scars of attach- skeletal differences, birds and crocodilians ment of the muscles under study. share unique myological similarities. More- The methods employed in this study are over, most of the phylogenetic transforma- essentially the phylogenetic methods dis- tions implied by this hypothesis are reca- cussed by Wiley ('81), Raikow ('82) and Gau- pitulated in avian ontogeny. thier (in press). However, I follow the suggestion of Maddison et al. ('84) of employ- MATERIALS AND METHODS ing at least two consecutive outgroups to de- In order to confirm attributes of muscles termine polarity of character transformation. described in published accounts, I dissected Using these methods, for example, I view the deep thigh muscles in adult and sub- character states shared uniquely by birds and adult specimens of a number of avian spe- crocodilians, based on comparisons with Lep- cies, and in a young (22cm snout-vent length) idosauria and Chelonia; as derived states caiman. All materials dissected are from the that distinguish Archosauria among reptiles. spirit collections of the Departments of Orni- thology and Herpetology, National Museum RESULTS of Natural History, with the exception of a Introduction to the problem number of young (6 to 10 weeks) anatids, The avian muscles that have been the focus meleagridids, tetraonids, and phasianids ob- of controversy are derivatives of the embry- tained from markets in Washington, D.C. I onic deep dorsal mass of the thigh, which have relied on published accounts for details during development divides to produce up to of the myology of Sphenodun, (Gadow, 1882; five separate adult muscles (Romer, '27a). Osawa, 1898; Byerly '25) Chelonia (Gadow, Under current nomenclature (Vanden Berge, 1882; Zug, '71; Walker, '73)and Lacerta (Ga- '79) these are Mm. iliofemoralis externus, dow, 1882; Romer, '42). Skeletons of these iliofemoralis internus, and the three muscles taxa in the National Museum of Natural His- of the iliotrochantericus group, Mm. iliotro- 330 T. ROWE

IFE CR IFE E

/ PU A

IT M

II -1 'I

B C &

Fig. 2. Gallus. Lateral view of right pelvis and femur twisted outwards to show more clearly M. cuppedicus. of 8-week old chicken, showing only those muscles that CUP, cuppedicus (=iliofemoralis internus); FE, femur; differentiate from the embryonic deep dorsal mass. A) IFE CR, iliofemoralis cranialis (=iliotrochantericus cau- Superficial view. B) The Mm. iliofemoralis externus and dalis); IFE E, iliofemoralis externus; IL, ilium; IS, is- iliofemoralis cranialis (=iliotrcchantericus caudalis) chium; IT CR, iliotrochantericus cranialis; IT M, have been removed. C) Iliofemoralis and iliotrochanteri- iliotrochantericusmedius; PU, pubis. cus muscles have been removed, and knee has been

chanterici cranialis, medius, and caudalis a condition unique to squamates (Romer, '42). (Fig. 2). Only two muscles in non-avian Rep- Hence, the condition from which birds tilia have been regarded as in any way ho- evolved was one in which M. iliofemoralis mologous with the five bird muscles, namely was a single muscle, and M. PIFI was divided Mm. iliofemoralis and pubo-ischio-femoralis into two parts. internus [PIFI] (Gadow, 1882; Gadow and Se- Descriptions of the differentiation of the lenka, 1891; Romer, '23a, '27a, '27b, '42; thigh musculature in crocodilians, Sphene Walker, '77; Lance Jones, '79). In Sphenodon don, and turtles are not currently available, (Osawa, 18981, Squamata (Romer, '42), Che- so reptilian ontogenetic patterns can not yet lonia (Zug, '71; Walker, '73; see below) and be compared. However, comparison of their Crocodylia (Romer, '23a), M. iliofemoralis is adult attributes with those in birds does pro- a single muscle, while M. PIFI is divided into vide evidence for a minimum number of two bellies (Fig. 3). In some squamates, M. transformations in avian phylogeny, and the PIFI is divided into three bellies, but this is occurrence of these same transformations in EVOLUTION OF AVIAN DEEP THIGH MUSCLES 331

Fig. 3. Alligator. Right lateral view of pelvis and fe- removed, and the cut surface indicated by cross hatching mur showing deep dorsal thigh muscles. The M. iliofem- (after Romer, '23a). FE, femur; IFE, position of origin of oralis has been removed; its position of origin on the iliofemoralis; IL, ilium; IS, ischium; PIFI DO, pubo-is- lateral face of the ilium is indicated by the dotted line. chio-femoralis internus pars dorsalis; PIFI M, pubo-is- The femur has been cut across the shaft, its distal half chio-femoralis internus pars medialis; PU, pubis.

avian ontogeny provides independent corrob- cral vertebrae and onto adjacent parts of the oration that they occurred historically (Nel- carapace, in a condition unique to turtles. It son, '78; Fink, '82; DeQueiroz, '85; Kluge, inserts on the dorsal surface of the femoral '85). trochanter majoris and acts to abduct and Although there is general agreement that protract the femur (Zug, '71; Walker, '73). In these muscles share some kind of homologi- Trionychidae,M. iliofemoralis divides to form cal relationship, previous investigators dis- two heads with a common insertion, in a agree on precisely what that relationship is condition unique to this family (Zug, '71). As and imply different sets of historic transfor- in other Reptilia and Lissamphibia, but not mations (Gadow, 1880, 1882; Gadow and Se- mammals, the chelonian iliofemoralis is in- lenka, 1891; Romer, '23a,b, '42; Walker, '77; nervated by branches of both the femoral and Lance Jones, '79). These different hypotheses peroneal nerves (Gadow, 1882). may be evaluated by comparison with an The chelonian M. PIFI is divided into two estimate of the minimum number and kinds parts. These are referred to as the antero- of transformations that must have occurred ventral division and the posterodorsal divi- historically. This estimate is made below by sion (Zug, '71; Walker, '73). In all turtles the comparing adult muscles in Aves with those anteroventral division is a large and power- of other Reptilia. Historical transformations ful muscle that originates from the dorsal suggested by this comparison are then com- surface of the pubis and epipubic cartilage. pared to ontogenetic transformations occur- In cheloniids the anteroventral division may ring during early development of the chick. be divided into separate superficial and deep layers, and in pleurodires its origin may ex- Deep dorsal thigh muscles in adult Reptilia pand onto the plastron, but both of these Chelonia conditions are derived within Chelonia In both pleurodire and cryptodire turtles, (Walker, '73). The posterodorsal division orig- M. iliofemoralis is a single muscle that arises inates from one or more presacral vertebrae from the dorsolateral surface of the ilium, and costal plates and from the medial surface just dorsal to the acetabulum (Fig. 4). It may of the ilium. The two divisions pass together also expand craniad onto one or two presa- in front of the acetabulum to insert as a 332 T. ROWE A B C

IS PU EPC \ PlFl PD IS

Fig. 4. Pseudemys. Origins and insertions of deep dor- chium; PIFI, common insertion of anteroventral and pos- sal thigh muscles on pelvis and femur. A) Right lateral terodorsal divisions of pubo-ischio-femoralis internus; view of pelvis. B) Dorsomedial view of pelvis. C) Right PIFI AV, origin of anteroventral division of pubo-ischio- femur in dorsal view (after Walker, '73; Zug, "71). EPC, femoralis internus; PIFI PD, origin of posterodorsal di- epipubic cartilage; WE, iliofemoralis; IL, ilium; IS, is- vision of pubo-ischio-femoralis internus; PU, pubis. common tendon on the dorsal surface of the As in turtles, the M. PIFI in Sphenodon femoral shaft and trochanter minoris. As in and Squamata arises from the dorsal or in- other Reptilia, both divisions of M. PIFI are ner surface of the pubo-ischiadic plate. It is a innervated by branches of the femoral nerve large muscle that covers most of the dorsal (Gadow, 1882). surface of the pubis and cranial half of the Turtles are like birds but unlike other rep- ischium. Byerly ('25) reported that M. PIFI tiles in that the insertions of both Mm. ilio- is undivided in Sphenodon; however, Osawa femoralis and PIFI are on the proximal end (1898), using the name pubo-ischio-trochan- of the femur rather than on the shaft. How- tericus internus, described and illustrated a ever, when all of the character data pertinent separate small cranial division. Both divi- to reptilian relationships are taken into ac- sions pass in front of the pubis, lateral to the count (e.g., Gauthier et al., in press), it is pubic tuberosity, to insert on the dorsal sur- most parsimonious to conclude that this con- face of the middle third of the femoral shaft. dition evolved independently in turtles and In some squamates (e.g., Lacerta), M. PIFI is birds. divided into three parts, pars dorsalis, medialis, and ventralis (synonymous with M. PIFI Lepidosauria parts I, 11, and 111, respectively, of Romer, As in turtles, M. iliofemoralis in the lepi- '42). All three divisions protract and rotate dosaurs Sphenodon (Osawa, 1898; Byerly, the femur forward. The squamate M. PIFI '25) and Squamata (Romer, '42) arises from ventralis corresponds to the small cranial di- the lateral face of the ilium, immediately vision in Sphenodon, while the caudal divi- dorsal to the acetabulum (Fig. 5). It inserts sion in Sphenodon is itself divided in some on the caudal surface of the middle third of squamates to form Mm. PIFI dorsalis and the femoral shaft and abducts and rotates medialis. Based on positional criteria, the the femur forward. It receives dual innerva- anteroventral division of M. PIFI in turtles tion, from branches of the femoral and pero- is homologous with the large caudal division neal nerves. in Sphenodon and the undivided anlage of EVOLUTION OF AVIAN DEEP THIGH MUSCLES 333

A B~ C PlFl A IFE 1.... .

Dorsal Ventral

Fig. 5. Sphenodon. Origins and insertions of deep dor- of anterior and posterior divisions of pubo-ischio-femo- sal thigh muscles on pelvis and femur (after Gadow, ralis internus; PIFI A, origin of anterior division of M. 1882; Osawa, 1898). A) Right lateral view of pelvis. B) pubischio-femoralis internus; PIFI P, origin of poste- Dorsomedial view of pelvis. C) Right femur. WE, ilio- rior division of M. pub-ischiefemoralis internus; PU, femoralis; IL,ilium; IS, ischium; PLFI, common insertion pubis.

Mm. PIFI dorsalis and medius in squamates. As in turtles and lepidosaurs, the crocodi- The posterodorsal division of turtles is ho- lian M. PIFI is considerably larger than M. mologous with the M. PIFI ventralis of squa- iliofemoralis. It is divided into two parts, pars mates and the small cranial division of M. dorsalis and pars medialis (PIFI parts I1 and PIFI in Sphenodon (Table 2; Walker, '73). I, respectively, of Romer, '23a), having different origins and insertions. Unlike turtles and lepidosaurs, in which M. PIFI arises from the Crocodylia pubo-ischiadic plate, in crocodilians it arises In crocodilians, as in turtles and lepido- from beneath the vertebral column. Pars dor- saurs, M. iliofemoralis arises from a large salis lies entirely cranial to the acetabulum, part of the lateral face of the ilium, immedi- where it originates ventrally on the six pre- ately dorsal to the acetabulum Fig. 3). In sacral transverse processes. It splits distally Archosauria, the ilium is antero-posteriorly to insert in two separate points on the dorsal expanded over the condition in other reptiles and cranial surfaces of the femoral shaft, well and the muscles arising from the ilium are distal to the femoral head. Pars medialis correspondingly enlarged. The area of origin originates from the medial surface of the il- of M. iliofemoralis in both crocodilians and ium and ventral surfaces of the sacral ribs. birds is thus expanded, with its rear edge It passes around the front of the ilium to extending well caudal to the rear margin of insert distal to the insertion of pars dorsalis, the acetabulum. This muscle inserts along on the caudal surface of the femur. Its area the caudal edge of the femoral shaft, well of origin and belly lie medial to the belly of distal to the femoral head, between the two pars dorsalis. Both divisions serve to abduct heads of M. femorotibialis pig. 6).It receives the femur and rotate it upward, forward, and dual innervation, from branches of the femo- inward. As in other Reptilia, both parts of M. ral nerve of the crural plexus, and the pero- PIFI receive innervation from only the fem- neal nerve of the lumbar plexus (Gadow, oral nerve (Gadow, 1882; Romer, '23a). The 1882; Romer, '23a). From its position, M. ili- crocodilian M. PIFI medialis is homologous ofemoralis evidently serves to abduct and ro- with the anteroventral division of M. PlFI in tate the femur forward. Chelonia, the posterior division in Sphene 334 T. ROWE don, and the undivided anlage of Mm. PIFI dorsalis and medius in Squamata (Walker, '73). The crocodilian M. PIFI dorsalis is homologous with the posterodorsal division of Chelonia, the pars ventralis of Squamata, and the cranial division in Sphenodon (Table 2). Aves In birds, the ilium and sacrum are greatly expanded to either side of the acetabulum compared with the condition found in non- dinosaurian Reptilia (Romer, '23b). The ala preacetabularis of the ilium is expanded forward over what is the lumbar region of other Reptilia. As a result, the lumbar plexus in birds issues from between vertebrae that have become incorporated into the sacrum, and the ilium completely covers the area from which M. PIFI arises in crocodilians. The musculature originating from the lateral face of the ilium is correspondingly expanded. Unlike the condition of other Reptilia, there are up to five separate muscles in birds, all of which arise solely from the ilium. The M. iliotrochantericus cranialis is reported to be present in all birds (George and Berger, '66; but see below), where it originates on the ventrolateral edge of the ilium, a entirely cranial to the acetabulum (Fig. 2), and inserts on the trochanter femoris (Fig. 7). It rotates the femur forward and inward, and is innervated by a branch of the femoral nerve (Romer, '27a; George and Berger, '66). The M. iliotrochantericus medius is reported to be present in most but not all birds (see below). It originates from the ventrolat- era1 edge of the ilium, cranial to the acetabulum, and just caudal to the origin of iliotrochantericus cranialis. It inserts on the trochanter femoris. It performs the same action and has the same innervation as M. iliotrochantericus cranialis. When present, it may have an incompletely divided origin or a common tendon of insertion with M. iliotrochantericus cranialis. aE The muscle currently referred to as iliotrochantericus caudalis (e.g., Vanden Berge, '79; renamed below "iliofemoralis cranialis") is reportedly present in all birds (George and Berger, '66; but see below). It is quite large, taking broad origin from the fossa iliaca dorsalis of the large ala preacetabularis of the

ilium. Its area of origin lies adjacent to the r( acetabulum. The fibers of M. iliotrochanteri- E cus caudalis pass ventrolaterally and con- a verge toward their point of insertion on the EVOLUTION OF AVIAN DEEP THIGH MUSCLES 335

Anterior Dorsal Posterior Fig. 6. AZZzgator. Insertions of deep dorsal thigh muscles on left femur (after Romer, ’23a). WE, iliofemoralis; PIFI DO, pubo-ischio-femoralis internus pars dorsalis; PIFI M, pubo-ischio- femoralis internus pars medialis.

proximal end of the trochanter femoris. This muscle rotates the femur forward and in- IFE CR ward and receives dual innervation, from branches of the femoral and peroneal nerves (Romer, ’27a). The M. iliofemoralis externus also originates from the lateral surface of the ilium immediately dorsal to the acetabulum, and inserts on the trochanter femoris. This muscle is present in many but not all birds (see below). It rotates the femur forward and inward and also receives dual innervation, from branches of the femoral and peroneal nerves. The muscle currently referred to as iliofemoralis internus (renamed below “cuppedicus”) is present in nearly all birds. It is reportedly absent only in “Tauraco leucotis (Musophagidae), certain genera of Old World Lateral Medial cuckoos (Coua, Carpococcyx, Centropus, Chrysococcyx, Cuculus), Upupa epops, Indi- Fig. 7. Gallus. Insertions of deep dorsal thigh muscles cator uariegatus, [andl Eugenes fulgens” on left femur. CUP,cuppedicus (=iliofemoralis inter- (George and Berger, ’66, p. 418). It arises nus); IFE CR, iliofemoralis cranialis (=iliotrochanteri- from the ventral edge of the ilium, immedi- cu8 caudalis); IFE E, iliofemoralis externus; CR, IT to iliotrochankricus cranialis; p~ M, iliotro&antericus atelY crania1 to the acetabulum, and deep medius. the bellies of Mm. iliotrochanterici cranialis 336 T. ROWE and medius. It inserts in the medial surface occurred before complete division of the mus- of the femur, immediately distal to the in- cle origins had occurred. turned femoral head. It weakly adducts the From this comparison of adults alone, there femur and rotates it forward and outward, is no evidence for loss of any ancestral mus- and is innervated by a branch of the femoral cles during avian phylogeny. Neither is nerve. transformation of innervation or action suggested, because in all Reptilia, including Aves, these muscles receive only femoral and Comparison of adult Reptilia or peroneal innervation, and they perform Comparison of adult attributes in Aves similar ranges of action. with those of non-avian Reptilia indicates Hypotheses of homology that at least three kinds of phyletic transformation occurred during the evolution of There has been general agreement that the birds. avian M. iliofemoralis externus is homolo- 1)Increase in the number of muscles. This gous with M. iliofemoralis of other Reptilia is suggested because the five avian muscles (Gadow, 1880, 1882; Gadow and Selenka, are represented by only three muscles (M. 1891; Romer, ’23a, ’27a,b, ’42; Walker, ’77; iliofemoralis and two bellies of M. PIFI) in Lance Jones, ’79). Both have similar position Crocodylia, Sphenodon, and Chelonia. As of origin, dual innervation, and perform sim- discussed above, the presence of two heads in ilar ranges of action. Because in non-avian M. iliofemoralis of Trionychidae and three Sauria M. iliofemoralis inserts on the shaft divisions of M. PIFI in Squamata are condi- of the femur well distal to the head, this tions unique to these taxa. During avian his- hypothesis requires that its position of inser- tory, therefore, a minimum of two additional tion has shifted proximally in birds. This ap- divisions of the three ancestral muscles must pears likely because proximal migration of have occurred, to produce the five adult avian its insertion also occurs during early stages muscles. It is conceivable that the additional in avian ontogeny (see below). avian muscles migrated to this region from There is also general agreement that avian elsewhere during embryogenesis, but onto- M. iliofemoralis internus (renamed below genetic data discussed below refute this “cuppedicus”) is homologous with at least possibility. part of one of the divisions of M. PIFI of other 2) Shifts in the position of muscle insertion. Reptilia (Gadow, 1880,1882; Gadow and Se- This must have occurred because M. iliofe- lenka, 1891; Romer, ’23a, ’27a,b, ’42; Walker, moralis and all divisions of M. PIFI in Cro- ’77; Lance Jones, ’79). This hypothesis re- codylia and Lepidosauria insert on the fem- quires that during avian history the homolog oral shaft well distal to its head, whereas in of M. iliofemoralis internus shifted its inser- Aves all five insert more proximally, on or tion proximally, and that its position of ori- near the trochanter femoris. The proximal gin moved onto the ilium. As described below, insertion of the deep thigh rpuscles in Che- the phylogenetic shift of its insertion is re- lonia might superficially resemble the avian capitulated during avian ontogeny. The hy- condition, but this is a convergent develop- pothesized shift in origin is substantiated ment that was not present in the most recent only by adult morphology, however, because common ancestor that Chelonia shared with throughout ontogeny the entire deep dorsal Aves (see above). Hence, proximal migration mass takes origin from the lateral surface of of insertion position occurred at least three the ilium (Romer, 27a). times during the evolution of birds. However, Despite general agreement on the homol- this minimum number could occur only if the ogy of M. iliofemoralis internus (renamed be- insertions shifted proximally before the divi- low “cuppedicus”) with part of M. PIFI in sion of the distal ends of the muscles was other Reptilia, the developmental pathway complete. of iliofemoralis in birds has been controver- 3) Shifts in the position of muscle origin. sial. After studying development of the chick, Only one of the muscles under study (M. ili- Romer (‘27a) believed M. iliofemoralis inter- ofemoralis) takes origin from the lateral sur- nus to be a derivative of the embryonic deep face of the ilium in Crocodylia, Lepidosauria, dorsal mass. Later, after studying the devel- and Chelonia, but all five do in birds. This opment of Lacerta, he rejected this view difference requires a minimum of two muscle (Romer, ’42). Based on new ideas about the origin shifts, provided, however, that they homologies of the other avian deep thigh EVOLUTION OF AVIAN DEEP THIGH MUSCLES 337 muscle, Romer concluded that his earlier ob- iliofemoralis (Romer, ’27a, p. 375). He later servations were erroneous, and that M. ilio- believed he had confirmation of this deriva- femoralis internus must be derived from the tion in his study on the development of Lac superficial dorsal mass, not the deep dorsal erta, arguing that the “iliotrochanterici are mass. Romer’s second opinion has been the derived from the reptilian ilio-femoralis as most generally accepted of the two (e.g., their development and position posterior to Lance Jones, ’79). However, throughout avian the femoral nerve would suggest,” and “in ontogeny M. iliofemoralis internus origi- the chick the iliofemoralis internus is the nates from a deep position adjacent to the lone survivor of the pubo-ischio-femoralis in- acetabulum, and its insertion remains on the ternus” (Romer, ’42, pp. 280-281). This view proximal half of the femur. All of the undis- has been widely accepted (Galton, ’69; puted deep dorsal mass derivatives also orig- Walker, ’77; Lance Jones, ’79; Cooper, ’81). inate from a deep position adjacent to the Despite its popularity, this view requires a acetabulum and insert on the proximal half number of transformations for which there is of the femur. Together with M. iliofemoralis no corroborative evidence. As argued above, internus, they lie caudomedial to the course comparison of adult Reptilia provides direct of the femoral nerve through the thigh. In evidence of only two splitting events, three contrast, derivatives of the superficial dorsal insertion shifts, and two origin shifts in the mass originate far from the acetabulum, history of birds. But implicit in the view of either from the periphery of the ilium or Gadow and Selenka (1891) and Romer (‘42) pubis, or from the shaft of the femur. They are all these plus a number of additional insert on the tibia or fibula, not on the femur, transformations. First, these authors hypoth- and they lie craniolateral to the femoral esize the loss of M. PIFI dorsalis. Because the nerve. Romer’s first opinion, that M. iliofem- divided M. PIFI of other Reptilia would be oralis internus develops from the deep dorsal represented by a single muscle in Aves, a mass, thus appears more accurate. second transformation is required, an addi- The homology of the three iliotrochanteri- tional splitting event (for a total of three) cus muscles, and whether some part of M. transforming the undifferentiated M. iliofem- PIFI has been lost in birds, have been the oralis into avian Mm. iliofemoralis externus subject of debate. Gadow (1880) and Romer and the three iliotrochanterici. Thirdly, a (‘23a) concluded from similarities in position transformation of action is required because that the avian iliotrochantericus group and M. iliofemoralis is a strong abductor of the M. iliofemoralis internus are both homolo- femur, but Mm. iliotrochanterici cranialis gous with M. PIFI dorsalis of Crocodylia. But and medius perform no abduction, and in- later Gadow and Selenka (1891) argued that stead protract the femur and rotate it for- M. PIFI dorsalis must have been lost in birds, wards and inwards. Finally, M. iliofemoralis that the iliotrochantericus group is homolo- receives both femoral and peroneal innerva- gous with M. iliofemoralis in Crocodylia, and tion, but two of its hypothesized derivatives, that M. iliofemoralis internus is the sole rem- Mm. iliotrochanterici cranialis and medius, nant of M. PIFI in Aves. Their rationale was receive only femoral innervation. No obser- that M. PIFI dorsalis receives only femoral vations in adults require any of these trans- innervation and therefore could not be ho- formation hypotheses, nor has evidence mologous with the iliotrochantericus group, been found to substantiate them in avian because iliotrochantericus caudalis receives ontogeny. both femoral and peroneal innervation. The source of this problem appears to be Romer (‘42) also later changed his opinion the assumption that the three muscles of the to defend the view of Gadow and Selenka iliotrochantericus group together form a nat- (1891), that M. PIFI dorsalis was lost, and ural unit that is uniquely differentiated from that the avian iliotrochantericus group is ho- a single homologous representative in other mologous with M. iliofemoralis of Lepidosau- Reptilia. All previous students have sought ria and Crocodylia. He had already pointed a single homolog for the three avian iliotro- out that in the developing chick Mm. iliotrochantericus muscles. But the evidence cur- chantericus caudalis and iliofemoralis exter- rently available argues for homology of M. nus differentiate from their common anlage iliofemoralis with only M. iliotrochantericus relatively late in ontogeny, suggesting to caudalis, not with all three of the iliotrochan- him, admittedly inconclusively, that the ilio- tericus muscles. Only when this hypothesis trochantericus group was derived from M. is extended to include Mm. iliotrochanterici 338 T. ROWE

DDM

-/ \FE IS Fig. 8. Pelvic region of embryonic chick early on the Fig. 9. Deep dorsal thigh musculature of embryonic sixth day of development. The superficial muscle mass chick late on the sixth day of incubation (stage III) (&r has been removed to show the undifferentiated deep Romer, ’27a). CUP, cupped~cus;WE, iliofemoralis (undif- dorsal mass (after Romer, ’27a). Drawings of embryos ferentiated), IT, iliotrochantericus (undifferentiated). are not to scale. D D M, deep dorsal mass; FE, femur; IL, ilium; IS, ischium; N FE, femoral nerve; N PR, peroneal nerve; N TB, tibia1 nerve; PU, pubis.

cranialis and medius must one assume the cleaves in an orderly pattern to produce up additional transformations described above. to five adult muscles. The first division is a The most parsimonious hypothesis sup- cleavage along a horizontal plane that di- ported by the characters described above is vides the early myoblastic condensation into that avian Mm. iliotrochantericus caudalis dorsal and ventral masses situated on either (renamed below “iliofemoralis cranialis”) and side of the primordium of the femur. By early iliofemoralis externus are homologous with on the sixth day of development (Romer’s M. iliofemoralis in other Reptilia, and that stage 11) the dorsal mass has itself divided into avian Mm. iliotrochanterici cranialis and separate superficial and deep masses. The medius are homologous with the single divi- deep mass at this stage receives innerva- sion of M. PIFI in other Reptilia that is the tion only from a twig of the femoral nerve equivalent of crocodilian M. PIFI dorsalis. As passing from in front of the acetabulum) discussed earlier, avian M. iliofemoralis in- (Fig. 8). ternus (renamed below %uppedicus”) is ho- By late on the sixth day (Romer’s stage 111), mologous with the single division of M. PIFI the deep dorsal mass has begun to differen- in other Reptilia that is equivalent to the tiate (Fig. 9). A broad cleft at their common crocodylian M. PIFI pars medialis (Table 2). origin distinguishes a cranial (preaxial) from This hypothesis requires only the seven a caudal (postaxial) mass. At this stage a transformations described above, whereas twig from the peroneal nerve can be seen the competing hypotheses require additional passing around the posterior edge of the pel- steps. A test of this hypothesis can be found vis to innervate the caudal mass. Cranially, in avian ontogeny. As discussed below, five differentiation proceeds more rapidly, and M. of the seven inferred phylogenetic transfor- iliofemoralis internus (renamed below “cup- mations are recapitulated. pedicus”) has separated along most of its length but maintains a common origin with Development of deep thigh muscles in the chick the cranial mass. On the sixth day, it inserts on a point about half-way down the femur, The following account is based on Romer’s but during subsequent developmental stages (’27a) study on the ontogeny of the chick. (Figs. 10, 11) the insertion migrates proxi- During early ontogeny, myoblastic mesen- mally, until it reaches its adult position im- chyme accumulates in the limb bud and then mediately distal to the inturned femoral EVOLUTION OF AVIAN DEEP THIGH MUSCLES 339

Fig. 10. Deep dorsal thigh musculature of embryonic chick on seventh day (stage IV) (after Romer, ’27a). A) Superficial view. B) niofemoralis removed. CUP, cuppedicus; IFE,iliofemoralis (undifferentiated);lT CR, iliotrochantericus cranialis; lT M, iliotrochantericusmedius.

Fig. 11. Deep dorsal thigh musculature of embryonic removed. CUP, cuppedicus; IFE CR, iliofemoralis crani- chick on the eighth day (stage V) (after Romer, ’27a). A) alis; IFE E,iliofemoralis externus; IT CR, iliotrochanter- Superficial view. B) niofemoralis anterior and externus icus cranialis; IT M, iliotrochantericus medius. head. By the eighth day, the insertion of M. ent growth and differentiation patterns are iliofemoralisinternus ~‘cuppedicus’’)lies very also clearly evident. The cranial mass has near its adult position. This developmental grown very little in size since stage I11 but transformation recapitulates one of the phy- has differentiated rapidly, and Mm. iliotro- logenetic transformations suggested by com- chanterici cranialis and medius have sepa- parison of adult Reptilia. rated. Their differentiation into two separate On the seventh day (stage IV), the cranial muscles is from an anlage originating and caudal masses are fully differentiated throughout ontogeny entirely from the ilium. from each other, having separate origins, in- This division recapitulates another of the insertions and fiber directions Fig. 10). Differ- ferred phylogenetic transformations. The in- 340 T. ROWE sertions of both muscle masses lie distal to rate of the deep dorsal myoblastic tissue. If the positions they attain in subsequent de- this is true, the avian ilium may simply grow velopmental stages. The proximal migra- quickly forward over the ancestral lumbar tions of these insertions are also recapitu- region, covering the area where the divisions lations of historic transformations. The M. of M. PIFI historically arose, blocking pas- iliofemoralis internus (%uppedicus”) is also sage of the myoblastic tissue into its ances- completely separate at this stage and is ov- tral region of differentiation. erlapped proximally by the bellies of Mm. In each of the five characters in which the iliotrochanterici cranialis and medius. These transformations can be observed, it is possi- three muscles originate entirely cranial to the ble to view Aves as possessing both the prim- acetabulum and have the same innervations itive archosaurian condition, which obtains and positions relative to each other that the only during early ontogeny, and the derived, divisions of M. PIFI maintain throughout uniquely avian state. The ontogeny of these life in Crocodylia (compare Figs. 3 and lob). characters thus exhibits a taxic (set within This similarity in positional criteria is only set) relationship that reflects the position of temporary, however, and later in avian on- Aves as a group within the more inclusive togeny M. iliofemoralis internus (“cuppedi- taxon Archosauria. This is not an indication cus”) shifts to a position ventral to the other that crocodilians are ancestral to Aves, as muscles. some authors have recently argued (e.g., The caudal mass has the opposite growth/ Martin et al., ’80; Martin, ’83a,b). Rather, differentiation pattern. It has grown rapidly it attests that all archosaurs pass through in size since stage 111, but is little differen- similar early developmental stages that, in tiated. This mass will divide to become the Aves, may continue to change as ontogeny adult Mm. iliofemoralis externus and iliotro- progresses. chantericus caudalis (renamed below “iliofe- It is evident that the three iliotrochanteri- moralis cranialis”), and this division reca- cus muscles do not possess a common history pitulates another of the inferred historic after the sixth day of ontogeny. The diver- transformations. However, at stage IV both gence of their separate pathways is one of still have a common origin and insertion and the earliest events in the development of the are separated by only a slight cleft near their deep thigh muscles, occurring before any of origin. The caudal mass inserts on the shaft the individual iliotrochantericus muscles dif- of the femur well distal to the insertions of ferentiates (Fig. 12). Consequently, grouping Mm. iliotrochanterici cranialis and medius, these muscles under a single name has only far from the insertions on the trochanter fe- topographic significance. Previous authors moris attained by its adult derivatives. have also attached phylogenetic significance By the eighth day (stage V), the insertion to this grouping. In a phylogenetic context, of the caudal mass has shifted proximad, however, “iliotrochantericus group” is a mis- passing laterad to the insertions of Mm. ilio- nomer. The name itself appears to have been trochanterici cranialis and medius, and in- a principal source of confusion in under- serts in a new position proximal to them on standing the homologies of these muscles, the trochanter femoris. This recapitulates having led previous students to seek a single another of the inferred historic transforma- homolog for all three muscles. So that no- tions. At this time, Mm. iliofemoralis exter- menclature can more accurately reflect the nus and iliotrochantericus caudalis “ilio- homology of these structures, a revision is femoralis cranialis” have clearly begun to discussed below. differentiate but still have a common origin (Fig. 11). Deep thigh muscles within Aves Under the hypothesis of homology pro- Under previous views of deep dorsal thigh posed here, five of the seven transformations muscle homology, variations within and inferred in avian history from comparison of among avian species have been subject to adult Reptilia can be observed during devel- conflicting interpretations. McGowan (‘79), opment of the chick. The two recapitulations for example, reported that in one of two spec- that do not occur are the shifts in position of imens of Apteryx, M. iliotrochantericus med- origin onto the ilium of the homologs of the ius was present but M. iliotrochantericus two divisions of M. PIFI. The absence of these cranialis, a muscle usually present in Apte recapitulations may result from accelerated ryx and other ratites, was anomalously growth of the ilium, relative to the growth absent. Vanden Berge (’82) argued that EVOLUTION OF AVIAN DEEP THIGH MUSCLES 341

CUPPEDICUS

ILIOTROCHANTERICUS x-. DORSAL MASS CRANIALIS ILIOFEMORALIS 1“ < EXTERNUS Fig. 12. Ontogeny of the deep dorsal thigh musculature of the chick.

McGowan’s interpretation presented an un- Sphenodon, and Chelonia; hence its differ- usual situation because, when only one of entiation into the two iliotrochantericus these two muscles is present, as is the case muscles is a condition that evolved within in many birds, it is generally M. iliotrochan- Archosauria, following the divergence of tericus cranialis, while M. iliotrochantericus Aves and Crocodylia from their most recent medius is considered to be absent. Vanden common ancestor. Because Mm. iliotrochan- Berge (’82), however, also correctly indicated terici cranialis and medius generally differ- that when only one of the two muscles is entiate in Ratitae (Gadow, 1880; George and present, it is simply a matter of convention to Berger, ’661, as well as in most neognaths call it iliotrochantericus “cranialis” rather (George and Berger, ’66), this condition ap- than “medius,” and that the homology of the pears to have been the ancestral state for single muscle has never been determined. Aves rather than arising during subsequent Hudson (‘37) employed this convention when diversification within the group. he recommended addition to the phenetic The M. iliotrochantericus is undifferenti- “Garrod muscle formula” of variants of M. ated (“iliotrochantericus medius is absent”) iliotrochantericus medius, but not M. iliotro- in Sula, Fregata, Ardea, Butoroides, Sagit- chantericus cranialis, whose presence he con- tarius, Accipiter, Buteo, Aquila, Circus, Pan- sidered to be constant. George and Berger dion, Falco, Polihierq Fulica, Totanus, Uria, (‘66) also followed this convention in their Tauraco, Otis, Bubo, Chordeiles, Chaetura, choice of names. They argued, however, that and Cuculidae (George and Berger, ’66, p. situations where only one of these muscles is 392). Partial differentiation of the two has present are not a result of loss of the second also been described. For example, George and muscle, but instead represent fusion of the Berger (’66, p. 392) reported that “in the Sand- two. They claimed that “...the fusion of these hill Crane, Mm. iliotrochantericus anterior two muscles [Mm. iliotrochanterici cranialis et medius are separate at their origins only; plus medius] is an example of the tendency the bellies fuse distally and insert by a com- toward fusion of muscles which arise from mon wide (1.5 cm) aponeurosis. In the right contiguous areas and whose fibers are essen- hip of one specimen, the two muscles were tially parallel” (p. 392). Thus, when only one completely fused, so that the complex was of the two muscles is present, previous au- represented by a single muscle mass, arising thors have disagreed as to whether one mus- from the same area occupied by both muscles cle has been lost and if so, which, or whether in the other dissections.” Non-differentiation the two have fused. or partial differentiation of the two iliotro- In contrast to these views, comparison of chantericus muscles in these neognaths is adult attributes in birds with other reptiles probably a result of neoteny (e.g., Gould, ’77) and the early development in the chick sug- evolving within Aves. One reason for uncer- gests that when only one muscle is present, tainty, however, is that the timing of its dif- it is because the common anlage of Mm. il- ferentiation is known only in the chick. Until iotrochanterici cranialis and medius fails to the timing of this event is known from a differentiate during ontogeny. The homolog broader comparative sample, it remains pos- of these muscles is undivided in Crocodylia, sible that presence of the undifferentiated M. 342 T. ROWE iliotrochantericus simply reflects immatu- undifferentiated M. iliofemoralis (“iliofemo- rity of this character in the specimen at hand. ralis externus absent”) in “Spheniscus, Avian specimens are usually considered Podiceps, Columba, Zenaidura, Goura, Gal- “adult” if they have mature plumage. But licolumba, Didunculus, Cuculidae, Chor- because different anatomical systems de- deiles, Apus, Eugenes, Pharomachrus, velop at different rates, the presence of adult Chloroceryle, Momotus, Coracias, Euryste plumage may not necessarily indicate the mus, Upupa, Aceros, Indicator, Colaptes, cessation of muscular development in all Dendrocopos, Procnias, and all other passer- species. ines examined” (p. 393). This state is re- In light of the preceding argument, the cur- ported to be the general condition for rent nomenclatural convention of referring Piciformes (Swierczewski and Raikow, ’81) to the undifferentiated M. iliotrochantericus and Coraciiformes (Maurer and Raikow, ’81). as “iliotrochantericus cranialis” is seen in- From the distribution of M. iliofemoralis correctly to imply differentiation of two mus- and its derivatives alone, one might conclude cles, followed by loss of one of them or fusion that Passeriformes, Piciformes, and Coraci- of the two. When only one muscle is present, iformes are primitive among birds, because it may be referred to simply as “iliotrochan- they share the same condition (non-division tericus.” This nomenclature serves more ac- of M. iliofemoralis)found in Crocodylia, Lep- curately to distinguish the single muscle idosauria, and Chelonia, whereas in other from its two derivatives, Mm. iliotrochanter- birds M. iliofemoralis is divided. However, icus cranialis and iliotrochantericus medius, because they also possess many other char- and reflects the hierarchies of muscle ontog- acters that are derived within Aves (e.g., Rai- eny and phylogeny. The M. iliotrochanteri- kow, ’82), there is general agreement that cus caudalis, however, shares neither unique passerines are highly derived among birds; phylogenetic nor ontogenetic history with it has never been suggested that passerines Mm. iliotrochanterici cranialis or medius, but are the plesiomorphic sister group to all other it does share a unique common pathway with living birds (e.g., Mayr and Amadon, ’51; M. iliofemoralis externus during both ontog- Wetmore, ’60; Feduccia, ’80; Cracraft, ’81). eny and phylogeny. Accordingly, I suggest Consequently, it is most parsimonious to that it be renamed “iliofemoralis cranialis” view differentiation of Mm. iliofemoralis (see below), to reflect more accurately both cranialis and externus as a derived condition its phylogeny and ontogenetic pathway, and for Aves generally, distinguishing Aves from to avoid confusion with M. iliotrochantericus other reptiles, and that the condition in pas- and its two derivatives. serine birds evolved from this state (Raikow, Variations in the derivatives of the caudal ’82). division of the deep dorsal mass are currently It thus appears likely that non-differentia- referred to using a similar convention. In tion of M. iliofemoralis in Passeriformes, Pi- most %on-passerine” birds, including Rati- ciformes, and Coraciiformes is a reversal, tae (Gadow, 1880) and Tinami (George and evidently the result of a neotenic truncation Berger, ’66), the caudal mass divides to form of the primitive avian ontogenetic pathway Mm. iliofemoralis externus and iliofemoralis of these muscles (Raikow, ’75; Raikow et al., cranialis (=“iliotrochantericus caudalis”). In ’79; Hall, ’84).This interpretation is further adult passerines and a few %on-passerines,” supported by the anomalous occurrence of M. the caudal mass fails to divide and only a iliofemoralis externus in one or a very few single muscle is present. When this is the specimens of several passerines species. It case, the single muscle has been called “il- was reported in the sturnids Acridotheses iotrochantericus caudalis,” and iliofemoralis tristis (Raikow, ’75) and Leucopsar roths- externus is said to be absent. In light of the childi (Raikow, et al., ’791, the bowerbird ontogenetic and phylogenetic histories de- Chlamydera nuchalis (Ptilonorhynchidae), scribed above, this convention is also mis- two species of Epimachus and Loria loriae leading. The single, undifferentiated muscle (both Paradisaeidae), and the turnagrid Tur- can most accurately be called M. “iliofemo- nagra capensis (Raikow et al., ’79). Its pres- ralis,” and its derivatives, where present, can ence in these taxa suggests that the gene- be distinguished as iliofemoralis externus tic information and developmental pathway and iliofemoralis cranialis, the latter name leading to differentiation of Mm. iliofemor- replacing “iliotrochantericus caudalis” (see alis externus and cranialis is fully conser- below). George and Berger (’66) report the ved in birds generally, and that phenotypic EVOLUTION OF AVIAN DEEP THIGH MUSCLES 343 expression of this program is regulated het- rately referred to simply as “M. iliotrochan- erochronically (Raikow, ’75; Raikow et al., tericus.” The convention of referring to the ’79; Hall, ’84). undivided M. iliotrochantericus as “iliotrochantericus cranialis” is misleading and Nomenclature should therefore be abandoned in phyloge- In a comprehensive review of avian myo- netic studies. logical nomenclature, Vanden Berge (‘79, p. As discussed above, the muscle currently 175) concluded that the avian deep thigh referred to as “iliotrochantericus caudalis” musculature is second only to the muscles of shares with M. iliofemoralis externus a the hand for nomenclatural confusion. The unique pathway of development and descent. path toward a solution to this problem is I suggest that our current understanding can clearly marked by general agreement on more accurately be reflected by using the the goal of avian myological nomenclature. new name “iliofemoralis cranialis” to re- George and Berger (’66, p. 225) stated that place iliotrochantericus caudalis, while “Ideally every avian anatomist would like to maintaining the term “iliofemoralis exter- have a set of names which would indicate the nus” in its current usage. If undivided, the homology of each muscle, not only among all single muscle should be called “M. iliofemor- birds but also in other vertebrate classes.” alis.” In this way, the hierarchies of muscle Bock (‘74, p. 136) agreed, stating that “The ontogeny and phylogeny for the two iliotro- desired goal [of avian myological nomencla- chantericus muscles and the two iliofemo- ture] is to apply the same name to homolo- ralis muscles are preserved in a hierarchical gous anatomical features throughout birds, naming structure. or tetrapods, or even vertebrates if that is The last decision necessitates renaming M. possible.” More recently, in the introduction iliofemoralis internus because its ontogeny to the Nomina Anatomica Avium [NAA], and history are quite distinct from those of Baumel et al. (1979, p. ix) explained that “In the other “iliofemoralis” muscles. To main- all anatomical nomenclatures it seems to tain its present name would imply a false have been easier to defend the status quo identity, and this seems a greater evil than than to attack it . . . Nevertheless the NAA the inevitable disruption of changing its has eliminated some substantial errors in name. The disruption might be minimized if the prevailing usage, particularly those a previously used name could be resurrected, founded on inaccurate anatomical beliefs or but I have been unable to find a suitable incorrect homologies.” As argued above, cur- synonym. Yliacus” (Hudson, ’37; George and rent nomenclature does not accurately re- Berger, ’66) and “psoas” (Howell, ’38; Fisher, flect the homologies of the avian deep thigh ’46) were used in the past, but both names muscles. Moreover, this has proved a source imply identity of the avian muscle with the of misdirection at higher levels of study, lead- uniquely mammalian muscles for which the ing previous students to seek a single homo- names were coined. No evidence currently log in other Reptilia for all three of the so- supports this implication and, if homology is called iliotrochantericus muscles in Aves. to be the criterion for organizing nomencla- This in turn resulted in acceptance of a more ture, both are therefore misnomers when ap- complex view of the evolution of the avian plied to the avian muscle. As discussed above, thigh than is warranted by available data. “iliofemoralis internus” is homologous with Revision of the nomenclature of these mus- the one division of M. PIFI medialis in Cro- cles thus appears necessary. codylia, but using this name for the avian The nomenclature I recommend is pre- “iliofemoralis internus” would imply unique sented in Figure 12 and Table 1. Following relationship with the avian M. pubo-ischio- the arguments presented above, I suggest femoralis (= M. adductor longus et brews), that the names “iliotrochantericus crani- which greatly differs developmentally and alis” and “iliotrochantericus medius” be re- historically from the deep dorsal mass deriv- tained in their current usage, but that atives. There seems no choice but to coin a “iliotrochantericus caudalis” be dropped. The new name. Mm. iliotrochanterici cranialis and medius I take this course with reluctance, because share unique historical and ontogenetic it will be the fourth name to be applied to pathways, and this is accurately reflected in this single structure, and even this course their current nomenclature. However, when poses difficulties. Traditionally, muscle only one muscle is present, it is most accu- names are based on their position of origin 344 T. ROWE and insertion, or function. However, this (iliotrochanericus and cuppedicus) originate practice predates by centuries the theory of throughout ontogeny from the ilium. At no evolution and a historic conception of homol- stage of ontogeny examined here are the ogy (Russell, ’16). When these attributes are positions or relations of these avian muscles transformed between homologous muscles, or similar to those of PIFI in adult turtles or when non-homologous muscles evolve simi- lepidosaurs. However, early in avian ontog- lar attachments or functions, nomenclatural eny, Mm. iliotrochantericus and cuppedicus ambiguities such as the present one may re- bear unique resemblance to the divisions of sult. It is not surprising to find need of revi- M. PIFI of adult crocodilians in their fiber sion of nomenclature for muscles so named, directions, and positions relative to the ver- in order that their evolutionary histories may tebral column, lumbar plexus, and the other be more accurately depicted and studied. deep thigh muscles. Birds thus appear to con- Christening the muscle, i.e., naming it as an serve nearly all of the ancestral archosau- individual, rather than its individual attri- rian character states, although in many butes (which may transform without affect- species their expression is confined to early ing its individuality) seems the best solution. ontogeny, and later uniquely avian modifi- I suggest the name “Cuppedicus,” from the cations obscure the resemblance in adults. Latin “cuppedia” (also cupedo-), meaning tit- In Aves ancestrally, the embryonic deep bit or delicacy. This term alludes to the min- dorsal mass differentiated into five adult ute size and delicate structure of the muscle, muscles. The embryonic postaxial division of but without direct reference to other for- the deep dorsal mass differentiated to form mally named anatomical structures. Mm. iliofemoralis cranialis (= iliotrochantericus caudalis) and iliofemoralis externus, DISCUSSION while the preaxial portion divided twice, The ancestral state of the deep dorsal thigh forming Mm. iliotrochanterici cranialis and musculature in Reptilia is reflected in those medius, and cuppedicus (= iliofemoralis in- attributes still shared by adult turtles and ternus). The presence of five adult deriva- lepidosaurs. There was an undivided, dually tives of the deep dorsal mass is thus an innervated M. iliofemoralis, and the M. PIFI apomorphy diagnostic of Aves. Another state was divided into two bellies that both origi- derived for Aves is the relative size of the nated from the dorsal surface of the pubois- deep muscles. In all other reptiles, M. PIFI is chiadic plate. In some turtles both divisions a powerful muscle that is larger than M. of PIFI have expanded onto the shell, and in iliofemoralis, but in birds iliofemoralis is trionychids the iliofemoralis divides into two greatly expanded and relatively much larger heads, both of which are states unique to than the avian homologs of PIFI. Two addi- turtles. The ancestral reptilian condition was tional avian apomorphies are that the homo- inherited unchanged in Sauria and is largely logs of PIFI take origin entirely from the preserved in the extant Sphenodon. Division ilium, and that all five deep dorsal deriva- of PIFI into three parts occurs in some Squa- tives insert on the proximal-most part of the mata, but since this state is known only in femur, instead of on the femoral shaft, as in squamates, it cannot be construed as the another Sauria. These ancestral avian states cestral state for Sauria, Lepidosauria, Archo- are conserved and expressed in fully mature sauria, or Aves, as some authors have ratites, tinamous, and many neognaths. The suggested. presence of fewer than five muscles in some In ancestral Archosauria, all primitive rep- neognaths and occasional ratite specimens tilian attributes were conserved, except that probably represents a heterochronic pertur- both divisions of M. PIFI had shifted their bation of the fully conserved ancestral avian position of origin away from the pubois- developmental program. It may also be pos- chiadic plate. They probably originated be- sible in some instances that fewer than five neath the sacral and lumbar portions of the adult muscles simply reflects immaturity of vertebral column, with M. PIFI dorsalis over- the specimen at hand. lapping broadly the belly of M. PIFI medialis Previous interpretations of deep thigh mus- laterally, as in extant crocodilians and early cle homology promoted a view of the evolu- stages in ontogeny of the chick. In all birds, tion of the avian hip in which its muscles the ilium is expanded forward over the re- had been subject to possible losses, reappear- gion where M. PIFI originates in crocodili- ances, new appearances, fusions, changes in ans, and as a result its avian homologs innervation, and changes in action. This view EVOLUTION OF AVIAN DEEP THIGH MUSCLES 345 reflected an extremely plastic system, hav- Muskulatur des Beckens und der hintern Gliedmasse ing passed through a multitude of evolution- der Ratiten. Jena: Fischer. Gadow, H.F. (1882) Beitrage zur Myologie der hintern ary changes over its long history. However, Extremitat der Reptilien. Morphol. Jahrb. 7382466. it now appears more likely that the ancestral Gadow, H.F., and E. Selenka (1891) Vogel I. Anatom- reptilian state of the deep thigh musculature ischer Theil. In H.G. Bronn (ed): Klassen und Ordnun- is largely conserved in Archosauria. The an- gen des Thier-Reichs, in Wort und Bild. Vol. 6. Leipzig: Winter. cestral archosaurian condition is in turn Gaffney, E.S. (1980) Phylogenetic relationships of the largely conserved in Aves, though obscured major groups of amniotes. In A.L. Panchen (ed): The in adult birds by uniquely avian modifica- Terrestrial Environment and the Origin of Land Ver- tions. This interpretation suggests that few tebrates. London: Academic Press, pp. 593-610. myological changes accompanied the shift Galton, P.M. (1969) The Pelvic Musculature of the Dino- saur Hypsilophodon (Repti1ia:Ornithischia). Postilla from quadrupedality to bipedality, despite No. 131. the associated profound modification of the Gauthier, J.A. (1984) A Cladistic Analysis of the Higher skeleton. Systematic Categories of Diapsida. Ph.D Thesis, Uni- versity of California, Berkeley. 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