Phenotypic and evolutionary plasticity of body composition in rats selectively bred for high endurance capacity

Journal of Applied Physiology

Volumn 109, Issue 3, 2010, Pages 778-785

  Swallow, J G ^a   Wroblewska, A K ^a   Waters, R P ^a   Renner, K J ^a,b   Britton, S L ^c   Koch, L G ^c  

^a W O Farber Center for Civic Leadership   (United States)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Acclimation; Correlated response; Food consumption; Organ masses; Wheel running activity

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BODY COMPOSITION; CARDIOMEGALY; COGNITION; COMPARATIVE STUDY; EATING; ENDURANCE; FEMALE; GENETIC SELECTION; GENETICS; GENOTYPE; HYPERTROPHY; INTESTINE; LIVER; MALE; MOTOR ACTIVITY; PATHOLOGY; PHENOTYPE; RAT; RAT STRAIN; REGRESSION ANALYSIS; STOMACH; TIME;

ANIMALS; BEHAVIOR, ANIMAL; BODY COMPOSITION; CARDIOMEGALY; EATING; FEMALE; GENOTYPE; HYPERTROPHY; INTESTINES; LEAST-SQUARES ANALYSIS; LIVER; MALE; MOTOR ACTIVITY; PHENOTYPE; PHYSICAL ENDURANCE; RATS; RATS, INBRED STRAINS; SELECTION, GENETIC; STOMACH; TIME FACTORS; VOLITION;

EID: 77957114733     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01026.2009     Document Type: Article

References (57)

1. Allen DL, Harrison BC, Maass A, Bell ML, Byrnes WC, Leinwand LA. Cardiac and skeletal muscle adaptations to voluntary wheel running in the mouse. J Appl Physiol 90:1900-1908, 2001.
2. o2max response to exercise training: results from the HERITAGE Family Study. J Appl Physiol 87:1003-1008, 1999.
3. Chappell MA, Garland T, Robertson GF, Saltzman W. Relationships among running performance, aerobic physiology and organ mass in male Mongolian gerbils. J Exp Biol 210:4179-4197, 2007.
4. De Bono JP, Adlam D, Paterson DJ, Channon KM. Novel quantitative phenotypes of exercise training in mouse models. Am J Physiol Regul Integr Comp Physiol 290: R926-R934, 2006.
5. De Moor M H M, Liu YJ, Boomsma DI, Li J, Hamilton JJ, Hottenga JJ, Levy S, Liu XG, Pei YF, Posthuma D, Recker RR, Sullivan PF, Wang L, Willemsen G, Yan H, De Geus E J C, Deng HW. Genome-wide association study of exercise behavior in Dutch and American adults. Med Sci Sports Exerc 41:1887-1895, 2009.
6. Eikelboom R, Mills R. A microanalysis of wheel running in male and female rats. Physiol Behav 43:625-630, 1988.
7. Friedman WA, Garland T, Dohm MR. Individual variation in locomotor behavior and maximal oxygen consumption in mice. Physiol Behav 52:97-104, 1992.
8. Gebczynski AK, Konarzewski M. Locomotor activity of mice divergently selected for basal metabolic rate: a test of hypotheses on the evolution of endothermy. J Evol Biol 22:1212-1220, 2009.
9. 2 delivery. J Appl Physiol 101:1288-1296, 2006.
10. Hammond K, Diamond J. Limits to dietary nutrient intake and intestinal nutrient uptake in lactating mice. Physiol Zool 67:282-303, 1994.
11. Hammond KA, Konarzewski M, Torres RM, Diamond J. Metabolic ceilings under a combination of peak energy demands. Physiol Zool 67:1479-1506, 1994.
12. Hammond KA, Roth J, Janes DN, Dohm MR. Morphological and physiological responses to altitude in deer mice Peromyscus maniculatus. Physiol Biochem Zool 72:613-622, 1999.
13. Hammond KA, Szewczak J, Krol E. Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient. J Exp Biol 204:1991-2000, 2001.
14. Harri M, Dannenberg T, Oksanen-Rossi R, Hohtola E, Sundin U. Related and unrelated changes in response to exercise and cold in rats: a reevaluation. J Appl Physiol 57:1489-1497, 1984.
15. Harrison BC, Bell ML, Allen DL, Byrnes WC, Leinwand LA. Skeletal muscle adaptations in response to voluntary wheel running in myosin heavy chain null mice. J Appl Physiol 92:313-322, 2002.
16. Hayes JP, Garland T. The evolution of endothermy-testing the aerobic capacity model. Evolution 49:836-847, 1995.
17. 2 uptake in rats selectively bred for endurance running capacity. J Appl Physiol 93:1265-1274, 2002.
18. Houle-Leroy P, Garland T Jr, Swallow JG, Guderley H. Effects of voluntary activity and genetic selection on muscle metabolic capacities in house mice Mus domesticus. J Appl Physiol 89:1608-1616, 2000.
19. Howlett R, Gonzalez N, Wagner H, Fu Z, Britton S, Koch L, Wagner P. Skeletal muscle capillary and enzyme activity in rats selectively bred for running endurance. J Appl Physiol 94:1682-1688, 2003.
20. Koch L, Britton S. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 5:45-52, 2001.
21. Koch LG, Britton SL. Aerobic metabolism underlies complexity and capacity. J Physiol 586:83-95, 2008.
22. Konarzewski M, Diamond J. Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiol Zool 67:1186-1212, 1994.
23. Koteja P, Carter PA, Swallow JG, Garland T. Food wasting by house mice: variation among individuals, families, and genetic lines. Physiol Behav 80:375-383, 2003.
24. Koteja P, Swallow JG, Carter PA, Garland T. Energy cost of wheel running in house mice: implications for coadaptation of locomotion and energy budgets. Physiol Biochem Zool 72:238-249, 1999.
25. Koteja P, Swallow JG, Carter PA, Garland T. Maximum cold-induced food consumption in mice selected for high locomotor activity: implications for the evolution of endotherm energy budgets. J Exp Biol 204:1177-1190, 2001.
26. Ksiazek A, Czerniecki J, Konarzewski M. Phenotypic flexibility of traits related to energy acquisition in mice divergently selected for basal metabolic rate (BMR). J Exp Biol 212:808-814, 2009.
27. Ksiazek A, Konarzewski M, Lapo IB. Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 11:890-899, 2004.
28. 2max and running performance in rats. J Appl Physiol 68:400-403, 1990.
29. Lerman I, Harrison BC, Freeman K, Hewett TE, Allen DL, Robbins J, Leinwand LA. Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J Appl Physiol 92:2245-2255, 2002.
30. Lightfoot JT, Turner MJ, Pomp D, Kleeberger SR, Leamy LJ. Quantitative trait loci for physical activity traits in mice. Physiol Genomics 32:401-408, 2008.
31. Malisch JL, Breuner CW, Gomes FR, Chappell MA, Garland T Jr. Orcadian pattern of total and free corticosterone concentrations, corticosteroid-binding globulin, and physical activity in mice selectively bred for high voluntary wheel-running behavior. Gen Comp Endocrinol 156:210-217, 2008.
32. McDevitt RM, Speakman JR. Central limits to sustainable metabolic rate have no role in cold-acclimation of the short-tailed field vole (Microtus agrestis). Physiol Zool 67:1117-1139, 1994.
33. Morgan TJ, Garland T, Carter PA. Ontogenies in mice selected for high voluntary wheel-running activity. I. Mean ontogenies. Evolution 57:646-657, 2003.
34. National Research Council. Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press, 1996.
35. Naya DE, Bacigalupe LD, Bustamante DM, Bozinovic F. Dynamic digestive responses to increased energy demands in the leaf-eared mouse (Phyllotis darwini). J Comp Physiol [B] 175:31-36, 2005.
36. Nehrenberg DL, Hua K, Estrada-Smith D, Garland T, Pomp D. Voluntary exercise and its effects on body composition depend on genetic selection history. Obesity (Silver Spring) 17:1402-1409, 2009.
37. Noland RC, Thyfault JP, Henes ST, Whitfield BR, Woodlief TL, Evans JR, Lust JA, Britton SL, Koch LG, Dudek RW, Dohm GL, Cortright RN, Lust RM. Artificial selection for high-capacity endurance running is protective against high-fat diet-induced insulin resistance. Am J Physiol Endocrinol Metab 293: E31-E41, 2007.
38. Novak CM, Escande C, Gerber SM, Chini EN, Zhang M, Britton SL, Koch LG, Levine JA. Endurance capacity, not body size, determines physical activity levels: role of skeletal muscle PEPCK. PLoS One 4: e5869, 2009.
39. Perusse L, Tremblay A, Leblanc C, Bouchard C. Genetic and environmental influences on level of habitual physical activity and exercise participation. Am J Epidemiol 129:1012-1022, 1989.
40. Rankinen T, Bouchard C. Gene-physical activity interactions: overview of human studies. Obesity (Silver Spring) 16 Suppl 3: S47-S50, 2008.
41. Rhodes JS, Gammie SC, Garland T. Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 45:438-455, 2005.
42. Rice T, Despres JP, Daw EW, Gagnon J, Borecki IB, Perusse L, Leon AS, Skinner JS, Wilmore JH, Rao DC, Bouchard C. Familial resemblance for abdominal visceral fat: the HERITAGE Family Study. Int J Obesity 21:1024-1031, 1997. (Pubitemid 27462407)
43. Rodnick KJ, Henriksen EJ, James DE, Holloszy JO. Exercise training, glucose transporters, and glucose transport in rat skeletal muscles. Am J Physiol Cell Physiol 262: C9-C14, 1992.
44. Rodnick KJ, Reaven GM, Haskell WL, Sims CR, Mondon CE. Variations in running activity and enzymatic adaptations in voluntary running rats. J Appl Physiol 66:1250-1257, 1989.
45. Sherwin CM. Voluntary wheel running: a review and novel interpretation. Anim Behav 56:11-27, 1998.
46. Simonen RL, Perusse L, Rankinen T, Rice T, Rao DC, Bouchard C. Familial aggregation of physical activity levels in the Quebec Family Study. Med Sci Sports Exerc 34:1137-1142, 2002.
47. Stubbe JH, Boomsma DI, Vink JM, Cornes BK, Martin NG, Skytthe A, Kyvik KO, Rose RJ, Kujala UM, Kaprio J, Harris JR, Pedersen NL, Hunkin J, Spector TD, de Geus EJ. Genetic influences on exercise participation in 37, 051 twin pairs from seven countries. PLoS One 1: e22, 2006.
48. Swallow JG, Carter PA, Garland T Jr. Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28:227-237. 1998.
49. Swallow JG, Garland T Jr, Carter PA, Zhan WZ, Sieck GC. Effects of voluntary activity and genetic selection on aerobic capacity in house mice (Mus domesticus). J Appl Physiol 84:69-76, 1998.
50. Swallow JG, Koteja P, Carter PA, Garland T. Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity. J Exp Biol 202:2513-2520, 1999.
51. Swallow JG, Koteja P, Carter PA, Garland T Jr. Food consumption and body composition in mice selected for high wheel-running activity. J Comp Physiol [B] 171:651-659, 2001.
52. Swallow JG, Rhodes JS, Garland T. Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integr Comp Biol 45:426-437, 2005.
53. Waters RP, Renner KJ, Pringle RB, Summers CH, Britton SL, Koch LG, Swallow JG. Selection for aerobic capacity affects corticosterone, monoamines and wheel-running activity. Physiol Behav 93:1044-1054. 2008.
54. Wilmore JH, Despres JP, Stanforth PR, Mandel S, Rice T, Gagnon J, Leon AS, Rao DC, Skinner JS, Bouchard C. Alterations in body weight and composition consequent to 20 wk of endurance training: the HERI-TAGE Family Study. Am J Clin Nutr 70:346-352, 1999.
55. Wisloff U, Najjar SM, Ellingsen O, Haram PM, Swoap S, Al-Share Q, Fernstrom M, Rezaei K, Lee SJ, Koch LG, Britton SL. Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307:418-420, 2005.
56. Yano H, Yano L, Kinoshita S, Tsuji E. Effect of voluntary exercise on maximal oxygen uptake in young female Fischer 344 rats. Jpn J Physiol 47:139-141, 1997.
57. Zhan WZ, Swallow JG, Garland T Jr, Proctor DN, Carter PA, Sieck GC. Effects of genetic selection and voluntary activity on the medial gastrocnemius muscle in house mice. J Appl Physiol 87:2326-2333, 1999.