Gene loss, thermogenesis, and the origin of birds

Annals of the New York Academy of Sciences

Volumn 1289, Issue 1, 2013, Pages 36-47

  Newman, Stuart A ^a   Mezentseva, Nadezhda V ^a   Badyaev, Alexander V ^b  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b University of Arizona   (United States)

Author keywords

Glut4; Morphological novelty; Myostatin; Skeletal muscle; UCP1

Indexed keywords

GALECTIN; GROWTH FACTOR; INSULIN; MYOD PROTEIN; MYOGENIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TRANSCRIPTION FACTOR PAX7; UNCOUPLING PROTEIN 1; UNCOUPLING PROTEIN 2;

ADAPTATION; ARTICLE; BIRD; BONE DEVELOPMENT; CLADISTICS; EMBRYO DEVELOPMENT; GENE DELETION; GENE EXPRESSION; GENE LOSS; GENOME; HYPERPLASIA; MECHANICAL STRESS; NESTLING; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHYLOGENY; SARCOPLASMIC RETICULUM; SEASONAL VARIATION; SKELETAL MUSCLE; THERMOGENESIS;

AVES;

EID: 84879318233     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/nyas.12090     Document Type: Article

References (111)

1. Newman, S.A. 2011. Thermogenesis, muscle hyperplasia, and the origin of birds. Bioessays. 33: 653-656.
2. Mezentseva, N.V., J.S. Kumaratilake & S.A. Newman. 2008. The brown adipocyte differentiation pathway in birds: an evolutionary road not taken. BMC Biol. 6: 17. doi:10.1186/1741-7007-6-17
3. Nicholls, D.G. 2001. A history of UCP1. Biochem. Soc. Trans. 29: 751-755.
4. Cannon, B. & J. Nedergaard. 2004. Brown adipose tissue: function and physiological significance. Physiol. Rev. 84: 277-359.
5. Seki, Y. et al. 2003. Broiler chickens (Ross strain) lack insulin-responsive glucose transporter GLUT4 and have GLUT8 cDNA. Gen. Comp. Endocrinol. 133: 80-87.
6. Kaltner, H. & H.J. Gabius. 2012. A toolbox of lectins for translating the sugar code: the galectin network in phylogenesis and tumors. Histol. Histopathol. 27: 397-416.
7. Kawahara, T. & K. Saito. 1976. Genetic parameters of organ and body weights in the Japanese quail. Poult. Sci. 55: 1247-1252.
8. Janssen, I. et al. 2000. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J. Appl. Physiol. 89: 81-88.
9. Müller, G.B. 2003. Embryonic motility: environmental influences and evolutionary innovation. Evol. Devel. 5: 56-60.
10. Hohtola, E. & G.H. Visser. 1998. "Development of locomotion and endothermy in altricial and precocial birds." In Avian Growth and Development. J.M. Starck & R.E. Ricklefs, Eds.: 157-174. New York, Oxford: Oxford University Press.
11. Herring, S.W. 1994. "Development of functional integration between skeletal and muscular system." In Bone: Differentiation and Morphogenesis of Bone, Vol. 9. B.K. Hall, Ed.: 165-191. Boca Raton: CRC Press.
12. Starck, J.M. 1994. Quantitative design of the skeleton in bird hatchlings: does tissue compartmentalization limit posthatching growth rates? J. Morphol. 222: 113-131.
13. Jastroch, M. et al. 2005. Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol. Genomics. 22: 150-156.
14. Tine, M. et al. 2012. Genomic characterization of the European sea bass Dicentrarchus labrax reveals the presence of a novel uncoupling protein (UCP) gene family member in the teleost fish lineage. BMC Evol. Biol. 12: 62. doi: 10.1186/1471-2148-12-62
15. Schwartz, T.S., S. Murray & F. Seebacher. 2008. Novel reptilian uncoupling proteins: molecular evolution and gene expression during cold acclimation. Proc. Biol. Sci. 275: 979-985.
16. Chiari, Y. et al. 2012. Phylogenomic analyses support the position of turtles as the sister group of birds and crocodiles (Archosauria). BMC Biology. 10: 65. doi: 10.1186/1741-7007-10-65
17. Grigg, G.C., L.A. Beard & M.L. Augee. 2004. The evolution of endothermy and its diversity in mammals and birds. Physiol. Biochem. Zool. 77: 982-997.
18. von Praun, C. et al. 2001. Tissue-specific expression and cold-induced mRNA levels of uncoupling proteins in the Djungarian hamster. Physiol. Biochem. Zool. 74: 203-211.
19. Blaylock, M.L. et al. 2004. UCP3 expression during weight gain and loss, cold exposure, and fasting in the collared lemming. Obes. Res. 12: 1690-1697.
20. Barger, J.L., B.M. Barnes & B.B. Boyer. 2006. Regulation of UCP1 and UCP3 in arctic ground squirrels and relation with mitochondrial proton leak. J. Appl. Physiol. 101: 339-347.
21. Raimbault, S. et al. 2001. An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem. J. 353: 441-444.
22. Teulier, L. et al. 2010. Cold-acclimation-induced non-shivering thermogenesis in birds is associated with upregulation of avian UCP but not with innate uncoupling or altered ATP efficiency. J. Exp. Biol. 213: 2476-2482.
23. Bouillaud, F. 2009. UCP2, not a physiologically relevant uncoupler but a glucose sparing switch impacting ROS production and glucose sensing. Biochim. Biophys. Acta. 1787: 377-383.
24. Clerc, P. et al. 2007. Nitric oxide increases oxidative phosphorylation efficiency. J. Bioenerg. Biomembr. 39: 158-166.
25. Bedu, E. et al. 2002. Increased lipogenesis in isolated hepatocytes from cold-acclimated ducklings. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283: R1245-R1253.
26. Benistant, C. et al. 1998. Increased in vitro fatty acid supply and cellular transport capacities in cold-acclimated ducklings (Cairina moschata). Am. J. Physiol. 275: R683-R690.
27. Barré, H. et al. 1986. Multilocular adipocytes from muscovy ducklings differentiated in response to cold acclimation. J. Physiol. 375: 27-38.
28. 2+ transport proteins in cold-acclimating ducklings. Am. J. Physiol. 269: C955-C960.
29. Rosenberg, H. et al. 2007. Malignant hyperthermia. Orphanet. J. Rare. Dis. 2: 21. doi:10.1186/1750-1172-2-21
30. Barré, H., L. Bailly & J.L. Rouanet. 1987. Increased oxidative capacity in skeletal muscles from cold-acclimated ducklings: a comparison with rats. Comp. Biochem. Physiol. B. 88: 519-522.
31. Bal, N.C. et al. 2012. Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat. Med. 18: 1575-1579.
32. Toyomizu, M. et al. 2002. Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle. FEBS Lett. 529: 313-318.
33. Mujahid, A. et al. 2005. Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poult. Sci. 84: 307-314.
34. Visser, G.H. 1998. "Development of temperature regulation." In Avian Growth and Development. J.M. Starck & R.E. Ricklefs, Eds.: 117-156. New York, Oxford: Oxford University Press.
35. Dawson, W.R. & A.F. Bennett. 1980. Metabolism and thermoregulation in hatchling western gulls (Larus occidentalis livens). Condor 82: 103-105.
36. Choi, I.-H., R.E. Ricklefs & R.E. Shea. 1993. Skeletal muscle growth, enzyme activities, and the development of thermogenesis: a comparison between altricial and precocial birds. Physiol. Zool. 66: 455-473.
37. Ricklefs, R.E. & T. Webb. 1985. Water content, thermogenesis and growth rate or skeletal muscles in the European starling. Auk 102: 369-376.
38. Visser, G.H. & R.E. Ricklefs. 1993. Development of temperature regulation in shorebirds. Physiol. Zool. 63: 771-792.
39. Ono, Y., H. Iwamoto & H. Takahara. 1992. Degeneration of type I fibers in the chick brachial muscles during post-natal development. Anim. Sc. Tech. 63: 341-348.
40. Hirabayashi, M. et al. 2005. Transformation of skeletal muscle from fast- to slow-twitch during acquisition of cold tolerance in the chick. Endocrinology 146: 399-405.
41. Mujahid, A. 2010. Acute cold-induced thermogenesis in neonatal chicks (Gallus gallus). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 156: 34-41.
42. Grav, H.J. et al. 1988. Oxidative capacity of tissues contributing to thermogenesis in eider Somateria mollissima ducklings: changes associated with hatching. J. Comp. Physiol. 158B: 513-518.
43. Steen, J.B. & G.W. Gabrielsen. 1986. Thermogenesis in newly hatched eider (Somateria mollissima) and long-tailed duck (Clangula hyemalis) ducklings and barnacle goose (Branta leucopsis) goslings. Polar Res. 4: 181-186.
44. Koskimies, J. & L. Lahti. 1964. Cold-hardiness of the newly hached young in relation to ecology and distribution in ten species of European ducks. Auk 81: 281-307.
45. Conejo, R. et al. 2001. Insulin produces myogenesis in C2C12 myoblasts by induction of NF-κB and downregulation of AP-1 activities. J. Cell. Physiol. 186: 82-94.
46. Gillespie, M.A. et al. 2009. p38-γ-dependent gene silencing restricts entry into the myogenic differentiation program. J. Cell. Biol. 187: 991-1005.
47. Santalucia, T. et al. 2001. A novel functional co-operation between MyoD, MEF2 and TRα1 is sufficient for the induction of GLUT4 gene transcription. J. Mol. Biol. 314: 195-204.
48. Nedachi, T., H. Fujita & M. Kanzaki. 2008. Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 295: E1191-E1204.
49. Sato, K. et al. 2012. Administration of insulin to newly hatched chicks improves growth performance via impairment of MyoD gene expression and enhancement of cell proliferation in chicken myoblasts. Gen. Comp. Endocrinol. 175: 457-463.
50. Buckingham, M. & F. Relaix. 2007. The role of Pax genes in the development of tissues and organs: Pax3 and Pax7 regulate muscle progenitor cell functions. Annu. Rev. Cell. Dev. Biol. 23: 645-673.
51. Picard, C.A. & C. Marcelle. 2013. Two distinct muscle progenitor populations coexist throughout amniote development. Dev. Biol. 373: 141-148.
52. Dupont, J., S. Tesseraud & J. Simon. 2009. Insulin signaling in chicken liver and muscle. Gen. Comp. Endocrinol. 163: 52-57.
53. Zhang, C.Y. et al. 2001. Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105: 745-755.
54. Ijiri, D. et al. 2009. Increased mass of slow-type skeletal muscles and depressed myostatin gene expression in cold-tolerant chicks. Zool. Sci. 26: 277-283.
55. Liknes, E.T. & D.L. Swanson. 2011. Phenotypic flexibility of body composition associated with seasonal acclimatization of passerine birds. J. Thermal Biol. 36: 363-370.
56. Vézina, F., A. Dekinga & T. Piersma. 2011. Shorebirds' seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together. Integr. Compar. Biol. 51: 394-408.
57. Swanson, D.L. et al. 2009. Seasonal variation of myostatin gene expression in pectoralis muscle of house sparrows (Passer domesticus) is consistent with a role in regulating thermogenic capacity and cold tolerance. Physiol. Biochem. Zool. 82: 121-128.
58. Nowell, M.M., H. Choi & B.C. Rourke. 2011. Muscle plasticity in hibernating ground squirrels (Spermophilus lateralis) is induced by seasonal, but not low-temperature, mechanisms. J. Comp. Physiol. B. 181: 147-164.
59. Starck, J.M. & R.E. Ricklefs. 1998. "Patterns of development: the altricial-precocial spectrum." In Avian Growth and Development. J.M. Starck & R.E. Ricklefs, Eds.: 3-30. New York, Oxford: Oxford University Press.
60. Ricklefs, R.E. 1983. Avian postnatal development. In Avian Biology, Vol. 7. D.S. Farner, J.R. King & K.C. Parkes, Eds.: 1-83. New York: Academic Press.
61. O'Connor, R.J. 1984. The Growth and Development of Birds. Chichester: Wiley.
62. Rahn, H., C.V. Paganelli & A. Ar. 1975. Relation of avian egg weight to body weight. Auk 92: 750-765.
63. Aulie, A. 1977. The effect of intermittent cold exposure on the thermoregulatory capacity of bantam chicks Gallus domesticus. Compar. Biochem. Physiol. A. 56: 545-549.
64. Visser, G.H. & R.E. Ricklefs. 1995. Relationship between body composition and homeothermy in neonates of precocial and semiprecocial birds. Auk 112: 192-200.
65. Hohtola, E. 2002. Facultative and obligatory thermogenesis in young birds: a cautionary note. Compar. Biochem. Physiol. A. 131: 733-739.
66. Moore, G.E. & G. Goldspink. 1985. The effect of reduced activity on the enzymatic development of phasic and tonic muscles in the chicken. J. Dev. Physiology. 7: 381-386.
67. Ricklefs, R.E., S. White & J. Cullen. 1980. Postnatal development of Leach's storm-petrel. Auk 97: 768-781.
68. Aulie, A. 1976. The pectoral muscles and the development of thermoregulation in chicks of Willow Ptarmigam (Lagopus lagopus). Compar. Biochem. Physiol. A. 53: 343-346.
69. Morton, M.L. & C. Carey. 1971. Growth and the development of endothermy in the mountain white-crowned sparrow (Zootrichia leucophrus oriantha). Physiol. Zool. 44: 177-189.
70. Olson, J.M. 1994. The ontogeny of shivering thermogenesis in the red-winged blackbird (Agelaius phoeniceus). J. Exp. Biol. 191: 59-88.
71. Visser, G.H. & R.E. Ricklefs. 1993. Temperature regulation in neonates of shorebirds. Auk 110: 445-457.
72. Whittow, G.C. & H. Tazawa 1991. The early development of thermoregulation in birds. Physiol. Zool. 64: 1371-1390.
73. Pedersen, H.C. & J.B. Steen. 1979. Behavioural thermoregulation in willow ptarmigan chicks Lagopus lagopus. Ornis. Scandinavica 10: 17-21.
74. Boersma, P.D. 1986. Body temperature, torpor, and growth of chicks of fork-tailed storm-petrels (Oceanodroma furcata). Physiol. Zool. 59: 10-19.
75. Koskimies, J. 1950. The life of swift, Micropus apus L. in relation to the weather. Ann. Acad. Sci. Fenn. A 15: 1-151.
76. Prinzinger, R. & K. Siedle. 1988. Ontogeny and metabolism, thermoregulation and torpor in the house martin Delichon urbica. Oecologia 76: 307-312.
77. Nowlan, N.C. et al. 2010. Mechanobiology of embryonic skeletal development: insights from animal models. Birth Defects Res. C. Embryo Today 90: 203-213.
78. Hall, B.K. & S.W. Herring. 1990. Paralysis and growth of the musculoskeletal system in the embryonic chick. J. Morphol. 206: 45-56.
79. Hall, B.K. 2001. Development of the clavicles in birds and mammals. J. Exp. Zool. 289: 153-161.
80. Bhat, R. et al. 2011. A regulatory network of two galectins mediates the earliest steps of avian limb skeletal morphogenesis. BMC Dev. Biol. 11: 6. doi: 10.1186/1471-213X-11-6.
81. Levi, G. & V.I. Teichberg. 1989. Patterns of expression of a 15K β-D-galactoside-specific lectin during early development of the avian embryo. Development 107: 909-921.
82. Hamburger, V. & H.L. Hamilton. 1951. A series of normal stages in the development of the chick embryo. J. Morphol. 88: 49-92.
83. Starck, J.M. 1996. Comparative morphology and cytokinetics of skeletal growth in hatchlings of alricial and precocial birds. Zool. Anz. 235: 53-75.
84. Starck, J.M. 1998. "Structural variants and invariants in avian embryonic and postnatal development." In Avian Growth and Development. J.M. Starck & R.E. Ricklefs, Eds.: 59-88. New York, Oxford: Oxford University Press.
85. Rot-Nikcevic, I. et al. 2007. Development of the mouse mandibles and clavicles in the absence of skeletal myogenesis. Histol. Histopathol. 22: 51-60.
86. Carter, D.R. & G.S. Beaupre. 2001. Skeletal Function and Form. Cambridge: Cambridge University Press.
87. Wong, M. & D.R. Carter. 2003. Articular cartilage functional histomorphology and mechanobiology: a research perspective. Bone 33: 1-13.
88. Hosseini, A. & D.A. Hogg. 1991. The effects of paralysis on skeletal development in the chick embryo. I: general effects. J. Anat. 177: 159-168.
89. Kablar, B. 2012. "Role of skeletal muscle in the epigenetic shaping of organs, tissues, and cell fate choices." In Epigenetics: Linking Genotype and Phenotype in Development and Evolution. B. Hallgrimsson & B.K. Hall, Eds.: 256-268. Berkeley: University of California Press.
90. Hosseini, A. & D.A. Hogg. 1991. The effects of paralysis on skeletal development in the chick embryo. II: effects on histogenesis of the tibia. J. Anat. 177: 169-178.
91. Müller, G.B. 1990. "Developmental mechanisms at the origin of morphological novelty: a side-effect hypothesis." In Evolutionary Innovations. M. Nitecki, Ed.: 99-130. Chicago: University of Chicago Press.
92. Hamburger, V. & R.W. Oppenheim. 1967. Prehatching motility and hatching behavior in the chick. J. Exp. Zool. 166: 171-204.
93. Slijper, E.J. 1942. Biologic-anatomical investigations on the bipedal gait and upright posture in mammals, with special reference to a little goat, born without forelegs. Proc. K. Ned. Akad. Wet. C. 45: 288-295, 407-215.
94. Le Maho, Y. et al. 1981. Body composition, energy expenditure, and plasma metabolites in long-term fasting geese. Am. J. Physiol. 241: E342-E354.
95. Cherel, Y., J.-P. Robin & Y. Le Maho. 1988. Physiology and biochemsitry of long-term fasting in birds. Canad. J. Zool. 66: 159-166.
96. Groscolas, R. 1986. Changes in body mass, body temperature and plasma fuel levels during the natural breeding fast in male and female emperor penguins Aptenodytes forsteri. J. Compar. Physiol. B 156: 521-527.
97. Robin, J.-P. et al. 1988. Protein and lipid utilization during long-term fasting in emperor penguins. Am. J. Physiol. 254: 61-68.
98. Badyaev, A.V. 1997. Avian life history variation along altitudinal gradients: an example with cardueline finches. Oecologia 111: 365-374.
99. Badyaev, A.V. & C.K. Ghalambor. 2001. Evolution of life histories along elevational gradients: evidence for a trade-off between parental care and fecundity in birds. Ecology 82: 2948-2960.
100. Piersma, T., G. A. Gudmundsson & K. Lilliendahl. 1999. Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72: 405-415.
101. Jenni, L. & S. Jenni-Eiermann. 1998. Fuel supply and metabolic constraints in migrating birds. J. Avian Biol. 29: 521-528.
102. Fry, C.H., I.J. Ferguson & R.J. Dowsett. 1972. Flight muscle hypertrophy and ecophysiological variation of yellow wagtail Motacilla flava races at Lake Chad. J. Zool. 167: 293-306.
103. Guglielmo, C.G., T. Piersma & T.D. Williams. 2001. A sport-physiological perspective on bird migration: Evidence for flight-induced muscle damage. J. Exp. Biol. 204: 2683-2690.
104. Gill, R.E.J. et al. 2005. Crossing the ultimate ecological barrier: evidence for an 11000-km-long nonstop flight from Alaska to New Zealand and eastern Australia by bartailed godwits. Condor 107: 1-20.
105. Gill, R.E.J. et al. 2009. Extreme endurance flights by landbirds crossing the Pacific Ocean: ecological corridor rather than barrier? Proc. R. Soc. Lond. B Biol. Sci. 276: 447-457.
106. Battley, P.F. et al. 2000 Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc. R. Soc. Lond. B Biol. Sci. 267: 191-196.
107. Georgiadis, V. et al. 2007. Lack of galectin-1 results in defects in myoblast fusion and muscle regeneration. Dev. Dyn. 236: 1014-1024.
108. Wilkins, A.S. 1997. Canalization: a molecular genetic perspective. Bioessays 19: 257-262.
109. Tudge, C. 2009. The Bird. New York: Three Rivers Press.
110. Mayr, E. 2001. What Evolution Is? New York: Basic Books.
111. Odling-Smee, F.J., K.N. Laland & M.W. Feldman. 2003. Niche Construction: The Neglected Process in Evolution. Princeton, NJ: Princeton University Press.