Evolution of muscle phenotype for extreme high altitude flight in the bar-headed goose

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1673, 2009, Pages 3645-3653

  Scott, Graham R ^a   Egginton, Stuart ^b   Richards, Jeffrey G ^a   Milsom, William K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY DEPARTMENT OF MEDICINE   (United Kingdom)

Author keywords

Exercise performance; High altitude adaptation; Oxygen transport cascade; Phylogenetically independent contrasts; Physiological evolution

Indexed keywords

ADAPTATION; ALTITUDE; BLOOD; EVOLUTIONARY BIOLOGY; FLIGHT; HYPOXIA; MITOCHONDRION; MUSCLE; PHENOTYPE; PHYLOGENETICS; PHYLOGENY; REACTION KINETICS; RESPIRATION; WATERFOWL;

AEROBIC CAPACITY; ALTITUDE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; FLIGHT MUSCLE; GOOSE; MITOCHONDRIAL VOLUME; MUSCLE MITOCHONDRION; NONHUMAN; OXYGEN DIFFUSION; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL;

ASIA; EURASIA; HIMALAYAS;

ANAS PLATYRHYNCHOS; ANSER; ANSER BRACHYRHYNCHUS; ANSER INDICUS; AVES; BRANTA LEUCOPSIS;

EID: 70350227347     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2009.0947     Document Type: Article

References (44)

1. Andrienko, T. et al. 2003 Metabolic consequences of functional complexes of mitochondria, myofibrils and sarcoplasmic reticulum in muscle cells. J. Exp. Biol. 206, 2059-2072. (doi:10.1242/jeb.00242)
2. Bassel-Duby, R. & Olson, E. N. 2006 Signaling pathways in skeletal muscle remodeling. Annu. Rev. Biochem. 75, 19-37. (doi:10.1146/annurev.biochem. 75.103004.142622)
3. Beall, C. M. 2007 Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc. Natl Acad. Sci. USA 104, 8655-8660. (doi:10.1073/pnas. 0701985104)
4. Biressi, S., Molinaro, M. & Cossu, G. 2007 Cellular heterogeneity during vertebrate skeletal muscle development. Dev. Biol. 308, 281-293. (doi:10.1016/j.ydbio.2007.06. 006)
5. Bishop, C. M., Butler, P. J., Egginton, S., Elhaj, A. J. & Gabrielsen, G. W. 1995 Development of metabolic enzyme activity in locomotor and cardiac muscles of the migratory barnacle goose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 38, R64-R72.
6. Bohonak, A. J. & van der Linde, K. 2004 RMA: software for reduced major axis regression, Java version 1.21. See http://www.kimvdlinde.com/ professional/rma.html.
7. Chappell, M. A. & Snyder, L. R. G. 1984 Biochemical and physiological correlates of deer mouse a-chain hemoglobin polymorphisms. Proc. Natl Acad. Sci. USA 81, 5484-5488. (doi:10.1073/pnas.81.17.5484)
8. Cramp, S. & Simmons, K. E. L. 1977 Handbook of the birds of Europe, the Middle East, and North Africa: the birds of the Western Palearctic. Oxford, UK: Oxford University Press.
9. Degens, H., Turek, Z., Hoofd, L. J., Van't Hof, M. A. & Binkhorst, R. A. 1992 The relationship between capillarisation and fibre types during compensatory hypertrophy of the plantaris muscle in the rat. J. Anat. 180, 455-463.
10. Deveci, D., Marshall, J. M. & Egginton, S. 2001 Relationship between capillary angiogenesis, fiber type, and fiber size in chronic systemic hypoxia. Am. J. Physiol. Heart Circ. Physiol. 281, H241-H252.
11. Egginton, S. 1990 Numerical and areal density estimates of fibre type composition in a skeletal muscle (rat extensor digitorum longus). J. Anat. 168, 73-80. (Pubitemid 20053151)
12. Faraci, F. M., Kilgore, D. L. & Fedde, M. R. 1984 Oxygen delivery to the heart and brain during hypoxia: pekin duck vs. bar-headed goose. Am. J. Physiol. 247, R69-R75.
13. Garland, T., Harvey, P. H. & Ives, A. R. 1992 Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18-32.
14. 2 in long axis of individual fibers in working dog gracilis muscle. Am. J. Physiol. Heart Circ. Physiol. 254, H1179-H1186.
15. Gnaiger, E. 2001 Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir. Physiol. 128, 277-297. (doi:10.1016/S0034-5687(01)00307-3)
16. Gnaiger, E., Méndez, G. & Hand, S. C. 2000 High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc. Natl Acad. Sci. USA 97, 11 080-11 085. (doi:10.1073/pnas. 97.20.11080)
17. Hochachka, P. W. 1985 Exercise limitations at high altitude: the metabolic problem and search for its solution. In Circulation, respiration, and metabolism (ed. R. Gilles), pp. 240-249. Berlin, Germany: Springer-Verlag.
18. Hochachka, P. W. & Burelle, Y. 2004 Control of maximum metabolic rate in humans: dependence on performance phenotypes. Mol. Cell. Biochem. 256, 95-103. (doi:10. 1023/B:MCBI.0000009861.45692.ed)
19. Hoppeler, H., Howald, H., Conley, K., Lindstedt, S. L., Claassen, H., Vock, P. & Weibel, E. R. 1985 Endurance training in humans: aerobic capacity and structure of skeletal muscle. J. Appl. Physiol. 59, 320-327.
20. Jessen, T.-H., Weber, R. E., Fermi, G., Tame, J. & Braunitzer, G. 1991 Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering. Proc. Natl Acad. Sci. USA 88, 6519-6522. (doi:10.1073/pnas.88.15.6519)
21. Kinsey, S. T., Hardy, K. M. & Locke, B. R. 2007 The long and winding road: influences of intracellular metabolite diffusion on cellular organization and metabolism in skeletal muscle. J. Exp. Biol. 210, 3505-3512. (doi:10.1242/ jeb.000331)
22. Lauder, G. V., Leroi, A. M. & Rose, M. R. 1993 Adaptations and history. Trends Ecol. Evol. 8, 294-297. (doi:10.1016/ 0169-5347(93)90258-Q)
23. Lee, S. Y., Scott, G. R. & Milsom, W. K. 2008 Have wing morphology or flight kinematics evolved for extreme high altitude migration in the bar-headed goose? Comp. Biochem. Physiol. C Pharmacol. Toxicol. 148, 324-331. (doi:10.1016/j.cbpc.2008.05.009)
24. León-Velarde, F., Sanchez, J., Bigard, A. X., Brunet, A., Lesty, C. & Monge, C. 1993 High altitude tissue adaptation in Andean coots: capillarity, fiber area, fiber type and enzymatic activities of skeletal muscle. J. Comp. Physiol. B 163, 52-58. (doi:10.1007/ BF00309665)
25. Maddison, W. P. & Maddison, D. R. 2009 Mesquite: a modular system for evolutionary analysis. Version 2.6. See http://mesquiteproject.org.
26. Mathieu-Costello, O. 2001 Muscle adaptation to altitude: tissue capillarity and capacity for aerobic metabolism. High Alt. Med. Biol. 2, 413-425. (doi:10.1089/ 15270290152608598)
27. Mathieu-Costello, O., Agey, P. J., Quintana, E. S., Rousey, K., Wu, L. & Bernstein, M. H. 1998a Fiber capillarization and ultrastructure of pigeon pectoralis muscle after cold acclimation. J. Exp. Biol. 201, 3211-3220.
28. Mathieu-Costello, O., Agey, P. J., Wu, L., Szewczak, J. M. & MacMillen, R. E. 1998b Increased fiber capillarization in flight muscle of finch at altitude. Respir. Physiol. 111, 189-199. (doi:10.1016/S0034-5687(97)00119-9)
29. McClelland, G. B., Hochachka, P. W. & Weber, J. M. 1998 Carbohydrate utilization during exercise after high-altitude acclimation: a new perspective. Proc. Natl Acad. Sci. USA 95, 10 288-10 293. (doi:10.1073/pnas.95.17. 10288)
30. Midford, P. E., Garland, T. & Maddison, W. P. 2005 PDAP Package of Mesquite. Version 1.07.
31. 2 affinity of animals living at high altitude. J. Appl. Physiol. 42, 139-143.
32. Rosser, B. W. C., Davis, M. B., Brocklebank, J. R. & George, J. C. 1987 On the histochemical characterization and distribution of fast and slow muscle fibers in certain avian skeletal muscles. Acta Histochem. 81, 85-93.
33. Scott, G. R. & Milsom, W. K. 2006 Flying high: a theoretical analysis of the factors limiting exercise performance in birds at altitude. Respir. Physiol. Neurobiol. 154, 284-301. (doi:10.1016/j.resp.2006.02.012)
34. Scott, G. R. & Milsom, W. K. 2007 Control of breathing and adaptation to high altitude in the bar-headed goose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R379-R391. (doi:10.1152/ajpregu.00161.2007)
35. Scott, G. R., Cadena, V., Tattersall, G. J. & Milsom, W. K. 2008 Body temperature depression and peripheral heat loss accompany the metabolic and ventilatory responses to hypoxia in low and high altitude birds. J. Exp. Biol. 211, 1326-1335. (doi:10.1242/jeb.015958)
36. Storz, J. F. & Moriyama, H. 2008 Mechanisms of hemoglobin adaptation to high altitude hypoxia. High Alt. Med. Biol. 9, 148-157. (doi:10.1089/ham. 2007.1079)
37. Suarez, R. K., Lighton, J. R., Brown, G. S. & Mathieu- Costello, O. 1991 Mitochondrial respiration in hummingbird flight muscles. Proc. Natl Acad. Sci. USA 88, 4870-4873. (doi:10.1073/pnas.88.11.4870)
38. Swan, L. W. 1970 Goose of the Himalayas. Nat. Hist. 70, 68-75.
39. Torrella, J. R., Fouces, V., Palomeque, J. & Viscor, G. 1998 Comparative skeletal muscle fibre morphometry among wild birds with different locomotor behaviour. J. Anat. 192, 211-222. (doi:10.1046/j.1469-7580.1998. 19220211.x) (Pubitemid 28241228)
40. Ward, S., Bishop, C. M., Woakes, A. J. & Butler, P. J. 2002 Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and barheaded geese (Anser indicus). J. Exp. Biol. 205, 3347-3356. (Pubitemid 35381016)
41. Weibel, E. R. 1979 Stereological methods. Toronto, Canada: Academic Press.
42. Weibel, E. R. 1984 The pathway for oxygen. Cambridge, MA: Harvard University Press.
43. Weibel, E. R., Taylor, C. R. & Hoppeler, H. 1991 The concept of symmorphosis: a testable hypothesis of structure - function relationship. Proc. Natl Acad. Sci. USA 88, 10 357-10 361. (doi:10.1073/pnas.88.22.10357)
44. Zhang, J., Hua, Z. Q., Tame, J. R. H., Lu, G. Y., Zhang, R. J. & Gu, X. C. 1996 The crystal structure of a high oxygen affinity species of haemoglobin (bar-headed goose haemoglobin in the oxy form). J. Mol. Biol. 255, 484-493. (doi:10.1006/jmbi.1996.0040) (Pubitemid 26105571)