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

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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 pectoralis, which raises the wings or paddles bipedality; brown fat; mechanobiology; plasticity; skeletal muscle; UCP1 . during flying and swimming, and the supracoracoideus (particularly extensive 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

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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 tetrapod clavicle would form in birds in which the developing primordia were subject to a balance of forces intermediate 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 postnatal 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 without 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 portions of mitochondrial uncoupling protein 1 features drove correlated changes in the thoracic skeleton that most dis- (UCP1), which in mammals uncouples others, with occupation of new ecologi- tinguish birds from other tetrapods are oxidative phosphorylation and is there-

654 Bioessays 33: 653–656,ß 2011 WILEY Periodicals, Inc...... Insights & Perspectives S. A. Newman

fore responsible for heat production [3, possibly secondary to alteration in the While the muscle hyperplasia hypo- 18]. Lizards also lack this gene, but fish distance between the primordia of the thesis addresses several long-standing and frogs have it (though none of these zeugopod [9]. It is plausible that some of puzzles, dispensing with the need to da Speculations & Ideas cold-blooded organisms have BAT), these lower limb modifications facili- provide adaptationist narratives for so the deletion most likely occurred in tated folding of the legs into an efficient incremental steps on the way to wings the reptilian lineage that included brooding posture, synergizing with the and indeed shifting the emphasis away theropod dinosaurs or their saurian heating effect of the increased muscle from the evolution of flight in the predecessors [3] (Fig. 1). mass. evolution of this clade, it raises its Neuroregulated thermogenesis is The imperative to increase skeletal own set of questions and speculations. an essential characteristic of all warm- muscle mass could now encompass How would the possibility that many blooded animals. In mammals, apart greatly enlarged pectorals (Fig. 1), shared skeletal characters of birds from BAT, this has its source in which would have compromised loco- and dinosaurs are plasticity-based increases in heart rate and shivering motion in quadrupeds. While the selec- homoplasies (i.e. outcomes of common in skeletal muscle [19]. In birds, tive pressure may have once more been formative principles), rather than ple- regulated thermogenesis depends for improved heat generation, the siomorphies (i.e. characteristics that largely on skeletal muscle, which is a enhanced size and strength of pectoral existed before divergence), affect views locus of nonshivering, as well as shiver- and biceps muscles would have enabled of the specific saurian ancestry of birds ing, thermogenesis [20, 21]. Bird body evolution of new functional modalities [1, 2]? Would support for this hypothesis (and egg incubation) temperatures are for the fore limbs. (Vestigiality of fore undermine the presumption that all around 39 8C; neonatal chicks are limbs was another option, given biped- swimming and flightless birds are unable to maintain this body tempera- ality.) The intermediate stages leading derived from volant progenitors? And ture by themselves for approximately a to the functionally transparent end- finally, is the extinction of nonavian week after hatching [22]. points of wings and paddles would no dinosaurs made more understandable For endothermic animals, the ability longer be enigmatic in this scenario. by the suggestion that these poikilother- to sustain elevated body temperatures Since selection was not initially for the mic and inadequately endothermic egg during the cooling of the late Jurassic adaptive efficacy of the limbs them- layers were muscled out by their hotter [23] would have been important to sur- selves, the suitability of the resulting relatives in a cooler world? vival. For the hatchlings of egg-laying appendages for flying or swimming endotherms (e.g. the ancestors of birds), could have been be a matter of niche it would have been a matter of life or occupation after the fact rather than Acknowledgments death. (Other egg-laying reptiles progressive refinement of a barely func- I have benefited from discussions with adopted poikilothermic strategies for tional structure [26]. Gerd Mu¨ller, Erica Newman, Kevin themselves and their offspring; mam- The shift to skeletal muscle as the Padian, and Sarah Werning. This work mals, in contrast, gestate internally major source of regulated heat gener- was supported in part by the National and their newborn, including human ation in evolutionary lineages lacking Science Foundation Frontiers in infants have ample stores of BAT.) UCP1 may have predisposed these Integrative Biology program. Modern birds brood both their eggs animals (beyond the described and hatchlings, and some theropod increases in muscle mass), to acquiring dinosaurs also apparently brooded their genetic variations supporting this func- References eggs [24]. This behavior has been dis- tion. Galliform birds and pigs (mammals cussed in relation to selection of long in which UCP1 is deleted or disrupted 1. Padian K, Chiappe LM. 1998. The origin and early evolution of birds. Biol Rev 73: 1–42. feathers in theropod dinosaurs [25], but [27]) are particularly susceptible to 2. Feduccia A. 1999. The Origin and Evolution it is clear that improving the means of malignant hyperthermia, a syndrome of Birds. New Haven: Yale University Press. heat generation would have been even in which skeletal muscles overheat p. 466. 3. Mezentseva NV, Kumaratilake JS, Newman more useful to brooding animals and due to genetic variants associated with SA. 2008. The brown adipocyte differentiation 2þ their hatchlings than added insulation. relaxed Ca regulation [28, 29]. pathway in birds: an evolutionary road not The saurian ancestors of modern In keeping with the perspective of taken. BMC Biol 6: 17. birds, insofar as they were endothermic, evolutionary-developmental biology, 4. Kaiser GW. 2007. The Inner Bird: Anatomy and Evolution. Vancouver: UBC Press. p. 386. would thus have been under strong the muscle hyperplasia hypothesis for 5. Gatesy S, Dial K. 1996. Locomotor modules selective pressure to increase their the origin of birds draws on both and the evolution of avian flight. Evolution 50: skeletal muscle mass. This was ‘‘internalist’’ and ‘‘externalist’’ modes 331–40. 6. Hou L, Martin LD, Zhou Z, Feduccia A. evidently realized first in the thigh of explanation [30], invoking develop- 1996. Early adaptive radiation of birds: evi- regions, leading to the side effect of mental plasticity for the generation of dence from fossils from northeastern China. upright posture, also found in many morphological novelties and natural Science 274: 1164–7. 7. Mu¨ ller GB., 1990. Developmental mechan- dinosaur groups. The embryological selection for gradual modification of isms at the origin of morphological novelty: a consequences of the increased forces existing characters (the thigh and breast side-effect hypothesis. In Nitecki M, ed; associated with larger thigh muscles muscles). Interestingly, in the scenario Evolutionary Innovations. Chicago: University would have included increases in long described, selection is driven by com- of Chicago Press. pp. 99–130. 8. 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656 Bioessays 33: 653–656,ß 2011 WILEY Periodicals, Inc. Corrigendum

To article: Thermogenesis, muscle hyperplasia, and the origin of birds, Newman, S. BioEssays Volume 33, Issue 9, pages 653–656, September 2011

DOI: 10.1002/bies.201100061

In the above article, the word ‘‘land’’ was inadvertently omitted from the third sentence, which should read: ‘‘The anatomical diversity of birds, the most species-rich and ecologically diverse of the land vertebrate classes, is remarkable.’’ In addition, the first sentence of the fifth paragraph contains a reversed attribution of the roles of the two major chest muscles of birds. The sentence should read: ‘‘The anterior locomotor module is associated with its own set of massive muscles, most prominently the pectoralis, which lowers the wings or paddles during flying and swimming, and the supracoracoideus (particularly extensive in penguins), which raises them.’’

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