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Thermogenesis, Muscle Hyperplasia, and the Origin of Birds

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Thermogenesis, Muscle Hyperplasia, and the Origin of Birds Volume 33 No. 9 September 2011 · ISSN 0265-9247 9/11 Ideas that Push the Boundaries Hypotheses Perspectives Reviews www.bioessays-journal.com Insights & Perspectives Ideas & Speculations Thermogenesis, muscle hyperplasia, and the origin of birds Stuart A. Newman A striking feature of all birds is the than flight itself, was the dominant arrangement, which is accompanied presence of massive skeletal muscles, theme in the transition from dinosaurs by an interruption in the overlying particularly as compared with related to birds. muscles, divides the bird body into taxa such as lizards or mammals. Birds are bipedal (as were their dino- relatively independent anterior and Depending on whether a bird is flight- saur ancestors), a condition inevitably posterior ‘‘locomotor modules’’ [5]. less or volant, a runner or swimmer, it associated with enlarged thigh muscles. Apart from the synsacrum and avian will have either hyperplastic thigh These are particularly massive in dino- hip, the posterior locomotor module muscles, breast muscles, or both. The saurs and flightless birds (Fig. 1). The contains several additional bird-specific anatomical diversity of birds, the most bipedality of birds, however, is distinct modifications of the pelvis and legs species-rich and ecologically diverse of from that inferred for any dinosaur, associated with unique functional adap- the vertebrate classes, is remarkable. being associated with unique skeletal tations. Unfused pubic bones permit the Nonetheless, the enormous, independ- modifications to the pelvis and the eggs of birds to be larger relative to body ently arising depots of skeletal muscle in bones of the lower limb. For example, size than those of any dinosaur. Plates of both the anterior and posterior body the femur is held nearly horizontal, and an expanded pelvic ischium define an regions represent, along with feathers its articulation with the pelvis (the avian abdominal vault that protects the elab- and beaks, a unifying motif across all hip) is essentially immobile, both owing orate digestive system (relative to other the specialized avian orders. While bird to the hyperplastic musculature [4]. reptiles), as well as the oviduct and evolution has generally been considered Birds have no separate lumbar eggs. In addition, the mentioned immo- to be driven by the evolution of feathers vertebrae. Instead, a synsacrum, con- bilization of the femur by the bulky and flight [1, 2], new evidence suggests sisting of a variable (depending on the musculature surrounding it has been that the loss of a single gene, that encod- species) group of lower vertebrae fused compensated by a unique specialization ing the mitochondrial uncoupling to each other and to the pelvis, exhibits of the avian leg in which skeletal novel- protein UCP1, in the reptilian ancestors independent mobility from the thoracic ties derived from fusion of ancestral of birds, led to crisis in which survival portion of the vertebral column at an bones, the tibiotarsus, syndesmosis of this lineage depended on marked interface referred to as the ‘‘lumbar’’ tibiofibularis, and tarsometatarsus, expansion of skeletal muscles [3]. The joint [4]. While some dinosaurs also mediate (along with their associated fact that the lineage did survive suggests had a synsacrum, fossil evidence for a muscles) locomotory patterns of walk- that this flight-enabling anatomical lumbar joint only appears with ances- ing, running, and swimming unlike and physiological specialization, rather tral birds, i.e. Archaeopteryx.This those of other tetrapods [4, 5]. The anterior locomotor module is associated with its own set of massive Keywords: muscles, most prominently the pector- alis, which raises the wings or paddles bipedality; brown fat; mechanobiology; plasticity; skeletal muscle; UCP1 . during flying and swimming, and the supracoracoideus (particularly exten- sive in penguins), which lowers them. DOI 10.1002/bies.201100061 Among the skeletal novelties of this region (aside from those of the highly Department of Cell Biology and Anatomy, New Abbreviations: disparate forelimbs, which became ves- York Medical College, Valhalla, NY, USA BAT, brown adipose tissue; UCP1, mitochondrial uncoupling protein 1. tigial in some dinosaurs and birds, and evolved into wings and paddles in other Corresponding author: Stuart A. Newman birds) are several unique structures of E-mail: [email protected] the thorax. These include the keel, an Bioessays 33: 653–656,ß 2011 WILEY Periodicals, Inc. www.bioessays-journal.com 653 S. A. Newman Insights & Perspectives ..... also those most dependent on muscular activity for their normal morphogenesis [8, 10, 13]. The clavicles, e.g., which are fused into the furcula in birds and some dinosaurs, were underdeveloped and unfused in chick embryos whose muscles were paralyzed [8, 10]. It is probable that the typical nonavian tet- rapod clavicle would form in birds in which the developing primordia were subject to a balance of forces intermedi- ate between that exerted by the bird musculature and the paralyzed state, i.e. the typical tetrapod configuration. The bipedal condition itself has developmental effects during the post- natal period, some of which echo the Ideas & Speculations novelties of avian skeletal anatomy. A dramatic demonstration of this comes from observations of a goat born with- out fore legs, described by Slijper [14], Figure 1. Schematic illustration of muscle hyperplasia hypothesis for the origin of birds. which learned to hop actively on its Animals represented in the red oval – bony fish, amphibians, and mammals – all have the gene hind legs. When dissected upon its for UCP1, although only mammals have thermogenic BAT. Animals represented in the blue accidental death at 1 year old, its mus- oval – birds and lizards – lack UCP1 and thus BAT. The common ancestor of lizards and birds, culoskeletal system exhibited a number and its dinosaur descendants, must also have lacked UCP1. The loss of UCP1 is presumed to of accommodations not characteristic have occurred within a group of tetrapods (represented by the animal in the purple sector) that contained ancestors of both saurians and mammals (which retained the gene). The muscle of goats, including a flattened and hyperplasia hypothesis asserts that selective pressure for maintenance of elevated body extended pelvic ischium. temperature of adults and particularly hatchlings in endothermic egg-laying saurian ancestors Explanations of bird origins based of birds in the absence of BAT led to increase in the mass of thermogenic thigh and breast on selection for suites of characters with muscles (pink). In consequence, descendents exhibited a bipedal stance and sustained ten- no evident functions in their incipient sion- and motility-based modifications in their developing skeletons, which generated numerous stages become unnecessary if bird- bird-specific novelties of the legs and thorax. specific skeletal novelties arose as side effects of hyperplastic skeletal muscles, either directly via forces exerted on the extension of the sternum unique to birds cal niches coming, in some cases, after developing skeleton during embryogen- [6], which provides an anchor for the the fact [7]. If this was indeed the esis, or indirectly via mechanical effects breast muscles, and the furcula (wish- trajectory of avian evolution, the char- on the immature postnatal skeleton. bone), formed by the fusion of the acters or functions that were modified But what evolutionary forces drove the clavicles. The latter was present in a during the early stages could not have muscle expansion? rudimentary form in some dinosaurs been directly related to the capacity of One peculiarity (relative to all and in Archaeopteryx, but only took ancestors to either fly or swim. other vertebrates) of the physiological on its definitive U shape in modern Focusing on embryonic develop- genetics of the reptilian ancestors of birds. The furcula is considered a stabi- ment provides an intrinsic connection birds indeed predisposed the endo- lizing adaptation for flight, so its pres- between increased muscle mass and therms among them to sustain a uni- ence in flightless dinosaurs has been the unique features of the avian directional increase in the mass of puzzling [1, 2]. skeleton. It is well documented that skeletal muscle. Birds have long been Evolutionary scenarios in which the mechanical activity of the embryo known to lack brown fat, a tissue that these innovations arose separately or is required for the ontogeny of the nor- generates heat in mammals [15]. Some coordinately by successive cycles of mal forms of many skeletal elements of avian species have aggregates of cells selection in an ancestral dinosaur line- vertebrates, particularly in birds ([8–11]; that resemble mammalian brown age, with anatomies adapted to flying, reviewed in refs. [12] and [13]). Paralyzed adipose tissue (BAT) [16, 17], and cells swimming, or bottom-heavy bipedality chick embryos fail to develop the fibular nearly identical to brown fat adipocytes (which seems antithetical to the first crest [9], which is a morphological nov- can be induced from chicken mesen- two) emerging at the end of multiple elty in theropod dinosaurs and a necess- chyme in vitro [3]. These tissues and millions of years of change, seem ary component in the development of cells are non-thermogenic, however, improbable. An alternative possibility the avian-specific syndesmosis tibiofi- since birds lack the nuclear gene for is that selection for a simpler array of bularis [7]. Moreover, those
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