Are voluntary wheel running and open-field behavior correlated in mice? different answers from comparative and artificial selection approaches

Behavior Genetics

Volumn 42, Issue 5, 2012, Pages 830-844

  Careau, Vincent ^a   Bininda Emonds, Olaf R P ^b   Ordonez, Genesis ^a   Garland Jr, Theodore ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

Anxiety; Cdh23ahl mutation; Comparative method; Experimental evolution; Exploration; Inbred strain

Indexed keywords

ALBINISM; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BIOLOGICAL TRAIT; BODY MASS; CAST MOUSE; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; HEARING LOSS; INBRED STRAIN; LOCOMOTION; MALE; MEASUREMENT ERROR; MOLF MOUSE; MOUSE; MUSCULAR DYSTROPHY; MUTATION; NONHUMAN; OPEN FIELD BEHAVIOR; PHYLOGENY; RETINA DEGENERATION; SINGLE NUCLEOTIDE POLYMORPHISM; SPRET MOUSE; THIGMOTAXIS; VOLUNTARY WHEEL RUNNING;

ANIMALS; BODY WEIGHT; DATA INTERPRETATION, STATISTICAL; DATABASES, GENETIC; FEMALE; MALE; MICE; MICE, INBRED STRAINS; MOTOR ACTIVITY; MUTATION; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; RUNNING; SELECTION, GENETIC; SEX CHARACTERISTICS; SPECIES SPECIFICITY;

MUS; RODENTIA;

EID: 84866550312     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-012-9543-0     Document Type: Article

References (90)

1. Archer J (1973) Test for emotionality in rats and mice: a review. Anim Behav 21:205-235
2. Ashton KG (2004) Comparing phylogenetic signal in intraspecific and interspecific body size datasets. J Evol Biol 17:1157-1161 (Pubitemid 39175183)
3. Atchley WR, Fitch WM (1991) Gene trees and the origins of inbred strains of mice. Science 254:554-558 (Pubitemid 21917371)
4. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125:279-284 (Pubitemid 33000466)
5. Blomberg SP, Garland T Jr, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717-745 (Pubitemid 36579712)
6. Bohren BB, Hill WG, Robertso A (1966) Some observations on asymmetrical correlated responses to selection. Genet Res 7:44-57
7. Boon AK, Réale D, Boutin S (2007) The interaction between personality, offspring fitness, and food abundance in North American red squirrel. Ecol Lett 10:1094-1104 (Pubitemid 47512356)
8. Boon AK, Réale D, Boutin S (2008) Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos 117:1321-1328
9. Boyer N, Réale D, Marmet J, Pisanu B, Chapuis JL (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538-547
10. Bronikowski AM, Carter PA, Swallow JG, Girard IA, Rhodes JS, Garland T Jr (2001) Open-field behavior of house mice selectively bred for high voluntary wheel-running. Behav Genet 31:309-316 (Pubitemid 33021071)
11. Bult A, Lynch CB (2000) Breaking through artificial selection limits of an adaptive behavior in mice and the consequences for correlated responses. Behav Genet 30:193-206
12. Burghardt PR, Fulk LJ, Hand GA, Wilson MA (2004) The effects of chronic treadmill and wheel running on behavior in rats. Brain Res 1019:84-96 (Pubitemid 39078614)
13. Butler MA, King AA (2004) Phylogenetic comparative analysis: a modeling approach for adaptive evolution.AmNat 164:683-695 (Pubitemid 40099523)
14. Butler D, Cullis BR, Gilmour AR, Gogel DJ (2007) ASReml-R reference manual Release 2.0. VSN International Ltd., Hemel Hempstead
15. Careau V, Réale D, Humphries MM, Thomas D (2010) The pace of life under artificial selection: personality, energy expenditure and longevity are correlated in domestic dogs. Am Nat 175:753-758
16. Careau V, Thomas D, Pelletier F, Turki L, Landry F, Garant D, Réale D (2011) Genetic correlation between resting metabolic rate and exploratory behaviour environment in deer mice (Peromyscus maniculatus). J Evol Biol 24:2153-2163
17. Crabbe JC, Phillips TJ, Kosobud A, Belknap JK (1990) Estimation of genetic correlation: interpretation of experiments using selectively bred and inbred animals. Alcoholism 14:141-151 (Pubitemid 20153355)
18. Crabbe JC, Wahlsten D, Dudek BC (1999) Genetics of mouse behavior: interactions with laboratory environment. Science 284:1670-1672 (Pubitemid 29291377)
19. Czesak ME, Fox CW, Wolf JB (2006) Experimental evolution of phenotypic plasticity: how predictive are cross-environment genetic correlations? Am Nat 168:323-335 (Pubitemid 44409578)
20. DeFries JC, Wilson JR, McClearn GE (1970) Open-field behavior in mice: selection response and situational generality. Behav Genet 1:195-211
21. Dewsbury DA (1980) Wheel-running behavior in 12 species of muroid rodents. Behav Proces 5:271-280
22. Dingemanse NJ, Both C, van Noordwijk AJ, Rutten AL, Drent PJ (2003) Natal dispersal and personalities in great tits (Parus major). Proc R Soc Lond B 270:741-747 (Pubitemid 36433927)
23. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM (2004) Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc Lond B 271:847-852 (Pubitemid 38491272)
24. Dixon LK, Van Mayeda D (1976) Effects of floor textures on openfield behavior in selected lines of mice. Behav Genet 6:87-92
25. Drager UC, Hubel DH (1978) Studies of visual function and its decay in mice with hereditary retinal degeneration. J Comp Neurol 180:85-114 (Pubitemid 8349306)
26. Droste SK, Gesing A, Ulbricht S, Muller MB, Linthorst ACE, Reul JMHM (2003) Effects of long-term voluntary exercise on the mouse hypothalamic- pituitary-adrenocortical axis. Endocrinology 144:3012-3023 (Pubitemid 36819903)
27. Duman CH, Schlesinger L, Russell DS, Duman RS (2008) Voluntary exercise produces antidepressant and anxiolytic behavioral effects in mice. Brain Res 1199:148-158
28. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman
29. Harlow Feder ME, Garland T Jr, Marden JH, Zera AJ (2010) Locomotion in response to shifting climate zone: not so fast. Annu Rev Physiol 72:167-190
30. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791
31. Fraser DF, Gilliam JF, Daley MJ, Le An N, Garrick TS (2001) Explaining leptokurtic movement distributions: intrapopulation variation in boldness and exploration. Am Nat 158:124-135 (Pubitemid 32682539)
32. Fuss J, Ben Abdallah NMB, Vogt MA, Touma C, Pacifici PG, Palme R, Witzemann V, Hellweg R, Gass P (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL/6J mice correlating with hippocampal neurogenesis. Hippocampus 20:364-376
33. Galis F, Van Der Sluijs I, Van Dooren TJM, Metz JAJ, Nussbaumer M (2007) Do large dogs die young? J Exp Zool (Mol Dev Evol) 308:119-126 (Pubitemid 46569737)
34. Gammie SC, Hasen NS, Rhodes JS, Girard I, Garland T Jr (2003) Predatory aggression, but not maternal or intermale aggression, is associated with high voluntary wheel-running behavior in mice. Horm Behav 44:209-221 (Pubitemid 37371976)
35. Garland T Jr, Dickerman AW, Janis CM, Jones JA (1993) Phylogenetic analysis of covariance by computer-simulation. Syst Biol 42:265-292
36. Garland T Jr, Bennett AF, Rezende EL (2005) Phylogenetic approaches in comparative physiology. J Exp Biol 208:3015-3035 (Pubitemid 41345680)
37. Garland T Jr, Kelly SA, Malisch JL, Kolb EM, Hannon RM, Keeney BK, Van Cleave SL, Middleton KM (2011a) How to run far: multiple solutions and sex-specific responses to selective breeding for high voluntary activity levels. Proc R Soc Lond B 278:574-581
38. Garland T Jr, Schutz H, Chappell MA, Keeney BK, Meek TH, Copes LE, Acosta W, Drenowatz C, Maciel RC, van Dijk G, Kotz CM, Eisenmann JC (2011b) The biological control of voluntary exercise, spontaneous physical activity and daily energy expenditure in relation to obesity: human and rodent perspectives. J Exp Biol 214:206-229
39. Gartner GEA, Hicks JW, Manzani PR, Andrade DV, Abe AS, Wang T, Secor SM, Garland T Jr (2010) Phylogeny, ecology, and heart position in snakes. Physiol Biochem Zool 83:43-54
40. Girard I, Garland T Jr (2002) Plasma corticosterone response to acute and chronic voluntary exercise in female house mice. J Appl Physiol 92:1553-1561 (Pubitemid 34670911)
41. Girard I, McAleer MW, Rhodes JS, Garland T Jr (2001) Selection for high voluntary wheel-running increases speed and intermittency in house mice (Mus domesticus). J Exp Biol 204:4311-4320 (Pubitemid 34861281)
42. Gould TD, Dao DT, Kovacsics CE (2009) The open field test. In: Gould TD (ed) Mood and anxiety related phenotypes in mice: characterization using behavioral tests. Humana Press, New York, pp 1-20
43. Hall CS (1934) Emotional behavior in the rat: defecation and urination as measures of individual differences in emotionality. J Comp Psychol 18:385-403
44. Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341-1351 (Pubitemid 27491132)
45. Hegmann JP, Possidente B (1981) Estimating genetic correlations from inbred strains. Behav Genet 11:103-114 (Pubitemid 11122657)
46. Ives AR, Midford PE, Garland T Jr (2007) Within-species variation and measurement error in phylogenetic comparative methods. Syst Biol 56:252-270
47. Johnson KR, Zheng QY, Erway LC (2000) A major gene affecting age-related hearing loss is common to at least ten inbred strains of mice. Genomics 70:171-180 (Pubitemid 32003394)
48. Jonas I, Schubert KA, Reijne F, Scholte J, Garland T Jr, Gerkema MP, Scheurink AJW, Nyakas C, van Dijk G (2010) Behavioral traits are affected by selective breeding for increased wheel-running behavior in mice. Behav Genet 40:542-550
49. Kirsten TB, Taricano M, Florio JC, Palermo-Neto J, Bernardi MM (2010) Prenatal lipopolysaccharide reduces motor activity after an immune challenge in adult male offspring. Behav Brain Res 211:77-82
50. Klomberg KF, Garland T Jr, Swallow JG, Carter PA (2002) Dominance, plasma testosterone levels, and testis size in house mice artificially selected for high activity levels. Physiol Behav 77:27-38 (Pubitemid 35245717)
51. Krebs CJ (1970) Microtus population biology: behavioral changes associated with the population cycle in M. ochrogaster and M. pennsylvanicus. Ecology 51:34-52
52. Lavin SR, Karasov WH, Ives AR, Middleton KM, Garland T Jr (2008) Morphometrics of the avian small intestine, compared with non-flying mammals: a phylogenetic perspective. Physiol Biochem Zool 81:526-550
53. Leasure JL, Jones M (2008) Forced and voluntary exercise differentially affect brain and behavior. Neuroscience 156:456-465
54. Lerman I, Harrison BC, Freeman K, Hewett TE, Allen DL, Robbins J, Leinwand LA (2002) Genetic variability in forced and voluntary endurance exercise performance in seven inbred mouse strains. J Appl Physiol 92:2245-2255 (Pubitemid 34666344)
55. Lightfoot JT, Leamy L, Pomp D, Turner MJ, Fodor AA, Knab A, Bowen RS, Ferguson D, Moore-Harrison T, Hamilton A (2010) Strain screen and haplotype association mapping of wheel running in inbred mouse strains. J Appl Physiol 109:623-634
56. Malisch JL, Breuner CW, Kolb EM, Wada H, Hannon RM, Chappell MA, Middleton KM, Garland T Jr (2009) Behavioral despair and home-cage activity in mice with chronically elevated baseline corticosterone concentrations. Behav Genet 39:192-201
57. Mather JG (1981) Wheel-running activity: a new interpretation. Mammal Rev 11:41-51
58. Meek TH, Lonquich BP, Hannon RM, Garland T Jr (2009) Endurance capacity of mice selectively bred for high voluntary wheel running. J Exp Biol 212:2908-2917
59. Miller BH, Schultz LE, Gulati A, Su AI, Pletcher MT (2010) Phenotypic characterization of a genetically diverse panel of mice for behavioral despair and anxiety. PLoS ONE 5:e14458
60. Nehrenberg DL, Hua K, Estrada-Smith D, Garland T Jr, Pomp D (2009) Voluntary exercise and its effects on body composition depend on genetic selection history. Obesity 17:1402-1409
61. Padilla E, Shumake J, Barrett DW, Holmes G, Sheridan EC, Gonzalez-Lima F (2010) Novelty-evoked activity in open field predicts susceptibility to helpless behavior. Physiol Behav 101:746-754
62. Parker HG, Kim LV, Sutter NB, Carlson S, Lorentzen TD, Malek TB, Johnson GS, DeFrance HB, Ostrander EA, Kruglyak L (2004) Genetic structure of the purebred domestic dog. Science 304:1160-1164 (Pubitemid 38661853)
63. Petkov PM, Ding Y, Cassell MA, Zhang W, Wagner G, Sargent EE, Asquith S, Crew V, Johnson KA, Robinson P, Scott VE, Wiles MV (2004) An efficient SNP system for mouse genome scanning and elucidating strain relationships. Genome Res 14:1806-1811 (Pubitemid 39276438)
64. Revell LJ, Harmon LJ, Collar DC (2008) Phylogenetic signal, evolutionary process, and rate. Syst Biol 57:591-601
65. Rezende EL, Chappell MA, Gomes FR, Malisch JL, Garland T Jr (2005) Maximal metabolic rates during voluntary exercise, forced exercise, and cold exposure in house mice selectively bred for high wheel-running. J Exp Biol 208:2447-2458 (Pubitemid 40912526)
66. Rhodes JS, Gammie SC, Garland T (2005) Neurobiology of mice selected for high voluntary wheel-running activity. Integr Comp Biol 45:438-455 (Pubitemid 41040139)
67. Rhodes JS, Ford MM, Yu CH, Brown LL, Finn DA, Garland T Jr, Crabbe JC (2007) Mouse inbred strain differences in ethanol drinking to intoxication. Genes Brain Behav 6:1-18 (Pubitemid 46090329)
68. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York
69. Rose MR (1984) Genetic covariation in Drosophila life history: untangling the data. Am Nat 123:565-569
70. Sherwin CM (1998) Voluntary wheel running: a review and novel interpretation. Anim Behav 56:11-27 (Pubitemid 28348956)
71. Shiotsugu J, Leroi AM, Yashiro H, Rose MR, Mueller LD (1997) The symmetry of correlated selection responses in adaptive evolution: an experimental study using Drosophila. Evolution 51:163-172
72. Sidman RL, Green MC (1965) Retinal degeneration in the mouse. Location of the rd locus in linkage group XVII. J Hered 56:23-29
73. Silver LM (1995) Mouse genetics: concepts and applications. Oxford University Press, New York
74. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690 (Pubitemid 44642609)
75. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758-771
76. Stanford SC (2007) The open field test: reinventing the wheel. J Psychopharm 21:134-135 (Pubitemid 46280460)
77. Stewart CC (1898) Variations in daily activity produced by barometric pressure and diet, with a description alcohol and by changes in of recording methods. Am J Physiol 1:40-56
78. Stone GN, Nee S, Felsenstein J (2011) Controlling for nonindependence in comparative analysis of patterns across populations within species. Philos Trans R Soc B 366:1410-1424
79. Swallow JG, Carter PA, Garland T Jr (1998) Artificial selection for increased wheel-running behavior in house mice. Behav Genet 28:227-237 (Pubitemid 28313461)
80. Swallow JG, Hayes JP, Koteja P, Garland T Jr (2009) Selection experiments and experimental evolution of performance and physiology. In: Garland T, Rose MR (eds) Experimental evolution: concepts, methods, and applications of selection experiments. University of California Press, Berkeley, pp 301-351
81. Swanson DL, Garland T Jr (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on presentday distributions. Evolution 63:184-194
82. Tarantino LM, Eisener-Dorman AF, Grabowski-Boase L, Steffy BM, Wiltshire T (2010) Quantitative trait locus and haplotype mapping in closely related inbred strains identifies a locus for open field behavior. Mamm Genome 21:231-246
83. Turner MJ, Kleeberger SR, Lightfoot JT (2005) Influence of genetic background on daily running-wheel activity differs with aging. Physiol Genomics 22:76-85 (Pubitemid 41356340)
84. van Overveld T, Matthysen E (2010) Personality predicts spatial responses to food manipulations in free ranging Great Tits (Parus major). Biol Lett 6:187-190
85. Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era-concepts and misconceptions. Nat Rev Genet 9:255-266
86. Wahlsten D, Bachmanov A, Finn DA, Crabbe JC (2006) Stability of inbred mouse strain differences in behavior and brain size between laboratories and across decades. Proc Natl Acad Sci USA 103:16364-16369 (Pubitemid 44715202)
87. Walsh RN, Cummins RA (1976) The open-field test: a critical review. Psychol Bull 83:482-504
88. Webster DG, Baumgardner DJ, Dewsbury DA (1979) Open-field behavior in eight taxa of muroid rodents. Bull Psychonom Soc 13:90-92
89. Wilson RC, Thomas V, Lanier DL, Dewsbury DA (1976) Open-field behavior in Muroid rodents. Behav Biol 17:495-506
90. Zombeck JA, DeYoung EK, Brzezinska WJ, Rhodes JS (2011) Selective breeding for increased home cage physical activity in collaborative cross and Hsd:ICR mice. Behav Genet 41: 571-582