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P0203-P0206.Pdf Condor, 81:203-206 0 The Cooper Ornithological Society 1979 THE EVOLUTIONARY RE-ESTABLISHMENT OF A LOST ANCESTRAL MUSCLE IN THE BOWERBIRD ASSEMBLAGE ROBERT J. RAIKOW STEPHEN R. BORECKY AND SUSAN L. BERMAN The loss of anatomical structures during the the New Zealand Thrush (Turnugra capensis; course of evolution is a common phenomenon, Turnagridae), the bellies of the IFE and M. and has elicited much discussion (see Regal iliotrochantericus caudalis are completely 1977 for a review of various theories of fused over most of their length and are causation). Many cases have been reported separate only at their insertions (Borecky in which lost ancestral structures have re- 1977 ) . appeared as developmental anomalies, but it We can offer three possible explanations is less often suggested that such ancestral for the presence of this muscle in the bower- characters can become re-established as nor- bird group. None of them can be either mal components of descendant groups, long totally refuted or verified, but we believe after their original loss. Such reversional that one hypothesis is by far the most likely phenomena have been attributed vaguely to for the reasons given below. These explana- the reversibility of mutations (e.g., Rensch tions follow. 1959:124), but advances in our understanding (1) Ancestral retention. It is possible that of how genes control development offer the IFE was never lost in the history of the insight into possible mechanisms for such bowerbird group, and that its presence is events. We report herein the apparent merely the retention of an ancestral character. re-establishment of a lost ancestral muscle This appears unlikely, however, because the in birds and speculate on the possible genetic muscle is lost in nearly all passerines, at least basis for it. as far as their myology is currently known, M. iliofemoralis externus (IFE), a small, as well as in several other groups of birds fan-shaped muscle of the hip in many non- generally considered to be closely related to passerine birds, arises on the ilium and inserts the Passeriformes, namely the Piciformes on the femur. In a group of related Aus- tralasian oscines there exists a muscle with ( Swierczewski 1977), the Coraciiformes and the form and position of the IFE, though this Trogoniformes (Maurer 1977), and the muscle has been found absent in other Pas- Cuculidae (George and Berger 1966:393). seriformes (George and Berger 1966:393; in Certainly the most parsimonious explanation that work the muscle is named M. gluteus for this distribution is that the IFE was lost medius et minimus). In the bowerbirds (Ptilonorhynchidae), wattlebirds ( Callaei- dae), and two species of sickle-billed birds- ILIUM of-paradise (Epimachus spp.; Paradisaeidae) this muscle arises fleshily from the caudal portion of the cranial iliac fossa and the caudal edge of the cranial iliac crest dorsal to the antitrochanter (Fig. 1). It is fused with the caudal edge of M. iliotrochantericus caudalis dorsally, but separates completely from that muscle a few millimeters proximal to the antitrochanter. The fleshy fibers of the IFE pass over the head of the femur and give rise to a short tendon that inserts on the caudolateral surface of the trochanter just proximal to the insertion of M. obturatorius FIGURE 1. Deep muscles of the hip in a bowerbird, lateralis pars dorsalis and caudal to the in- Chlamudera nuchalis. showing the relationshin of M. sertion of M. iliotrochantericus caudalis. In iliofemoralis externus ( IFE ) to M. iliotrochantericus caudalis (ITC) characteristic of the bowerbird assem- Lorias’ Bird-of-paradise (Lo&r lo&e) and blage. Compare with Figure 3. 12031 204 R. J. RAIKOW, S. R. BORECKY AND S. L. BERMAN in the common ancestor of this passerine and near-passerine assemblage. (2) Convergence. The muscle in the bower- bird group may be a newly evolved structure that mimics but is not homologous to the IFE of other groups. That is, it could be an in- dependently evolved structure whose ontog- eny is not controlled by a system of genes derived from that which controlled the development of the true IFE in ancestral forms. We consider this possibility unlikely because of the remarkable similarity in structure, position, and attachments of the muscle in the bowerbird group and in other birds. (3) Re-establishment. We favor the hy- pothesis that when the muscle was “lost” in FIGURE 2. Lateral view of deep thigh musculature the ancestry of the passerines, its loss was of a woodswallow, Artamus leucorhynchus, showing limited to its expression in the phenotype; the anomalous (unilateral) presence of M. iliofem- the genetic mechanism controlling its on- oralis. Abbreviations: CF,. G. caudofemoralis; FCM, M. flexor cruris medialis: FTE. M. femorotibialis exter- togenesis was retained though not expressed. nus; ILF, M. iliofemoralis (anomaly); ISF M. ischio- We present four arguments in support of this femoralis; ITCR, M. iliotrochantericus crakalis; PIF, hypothesis: M. pubo-ischiofemoralis. (a) Similarity. As noted above, the sim- ilarity of the muscles in the bowerbird group and various nonpasserines is so great that the regulatory systems rather than in the struc- control of its development by totally un- tural genes (e.g., Wilson 1976). The existence related genetic systems appears very unlikely. of developmental anomalies which revert to If such a great taxonomic gap in its occur- an ancestral structure supports this concept. rence did not exist, no question of homology Some examples were discussed previously would arise. ( Raikow 1975)) including myological ata- (b) Inactivation. The mechanisms con- visms in mammals, the occurrence of upper trolling loss and reappearance of structures incisors or canines in sheep, the retention of such as those reported herein and in the capabilities for directing tooth formation in literature reviewed below are, ultimately, the domestic chicken, and anomalous re- genetic in nature. We cannot present a appearances of muscles in birds. After that specific explanation on this level for such paper was written, we discovered the follow- phenomena, because the present understand- ing additional cases of the anomalous re- ing of the genetic control of development is appearance of ancestral muscles in individual still rudimentary. It is possible, however, to birds and mammals. speculate briefly within the context of cur- M. iliofemoralis (caudiliofemoralis pars rent genetic theory. There is ample evidence i2iofemoraZis). This thin, strap-shaped muscle that genetic mechanisms can be inactivated was found on the left side of one specimen of during the course of development. Indeed, a White-breasted Woodswallow ( Artamus current models of the genetic control of de- leucorhynchus; Artamidae; Fig. 2). It arose velopment in eukaryotes invoke the mecha- by a thin aponeurosis from the lateral surface nism of specific temporal patterns of gene of the dorsolateral iliac crest just cranial to activation and deactivation in differentiating the caudal margin of the origin of M. cell lineages (see Caplan and Ordahl 1978, ischiofemoralis. The parallel-fibered belly and references therein for discussions of passed craniodistally to insert tendinously on the caudolateral surface of the femur lateral various models). The details of such specu- to the insertion of M. caudofemoralis. The lative models need not be reviewed here; it muscle did not occur on the other side of this is sufficient for the present purpose to high- specimen, or on either side of another speci- light the critical idea that functionally related men of the same species. It is normally absent structural genes are controlled by families of in passerines. Another anomalous occurrence regulatory genes, and that much of the mor- of this muscle was previously reported in a phological change that occurs in the evolution Fox Sparrow (Passerella iliaca; Raikow 1975). of animals can be ascribed to changes in the M. iliofemoralis externus. We examined the RE-ESTABLISHMENT OF AN ANCESTRAL MUSCLE 205 IFE ITC FIGURE 3. Muscles of the hip in a specimen of a starling, Leucopsar ~othschilck The M. iliofemoralis externus (IFE) is an anomaly, and was absent on the other side of the specimen. ITC, M. iliotrochantericus caudalis. Compare with Figure 1. FIGURE 4. Muscles of the back in a Yellow-rumped Cacique ( Cacicus cela ) showing the presence of M. latissimus dorsi pars caudalis on the left side and its limb muscles of 20 genera of Sturnidae absence on the right side. The asymmetrical appear- ance is due to an oblique angle of view. LDC, M. (Borecky 1977) and found that the IFE is latissimus dorsi pars caudalis; LDCR. M. latissimus normally absent in this family. However, in dorsi pars cranialis. a Rothschilds’ Myna ( Leucopsar rothschildi), we found, on one side of the body, an anomalous IFE of the form normally present (Cacicus cela) the muscle was present bi- in the Australasian families described above, laterally in one specimen and unilaterally in i.e., partially fused to the iliotrochantericus another (Fig. 4). These observations support caudalis (Fig. 3). An anomalous occurrence the idea that the appearance or nonappear- of this muscle was previously described in ance of a muscle may depend on a relatively another sturnid, the Common Myna (Acrido- easily perturbed developmental event; in terms theres t&is; Raikow 1975). of current theory this may be attributable to M. abductor cruris caudalis. In a study of the switching on or off of a regulatory gene. the hind limb of bipedal rodents, this muscle (d) Anomulies in sturnids. We noted was found unilaterally in one of 18 specimens above two occurrences of the anomalous of the Egyptian Jerboa (Jaculus jaculus; presence of the IFE in different genera of Dipodidae) (Berman, unpubl. data). It was the family Sturnidae. This suggests that the also absent in 25 specimens in three genera developmental information for the growth of of other bipedal dipodoids. The origin, in- this muscle is present in an inactive state in sertion, and relationships of the muscle were this family, occasionally being expressed in similar in this specimen to the condition in anomalous individuals.
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