Sex differences in thermogenesis structure behavior and contact within huddles of infant mice

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Harshaw, Christopher ^a   Culligan, Jay J ^a   Alberts, Jeffrey R ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR; BROWN ADIPOSE TISSUE; COLD; CONTACT BEHAVIOR; DYNAMICS; FEMALE; GRANGER ANALYSIS; HUDDLE; INFANT; INFRARED PHOTOGRAPHY; INTERCAPSULAR TEMPERATURE; MALE; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PUP (RODENT); RATING SCALE; SCORING OF CONTACT; SCORING SYSTEM; SEX DIFFERENCE; SOCIAL INTERACTION; TEMPERATURE; THERMOGENESIS; THERMOREGULATION; WARMING;

ADIPOSE TISSUE, BROWN; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; MICE; RATS; SEX CHARACTERISTICS; THERMOGENESIS;

EID: 84900311423     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0087405     Document Type: Article

References (105)

1. Gordon CJ (2009) Quantifying the instability of core temperature in rodents. J Therm Biol 34: 213-219.
2. Gordon CJ (2012) The mouse: An "average" homeotherm. J Therm Biol 37: 286-290.
3. Gordon CJ (2012) Thermal physiology of laboratory mice: Defining thermoneutrality. J Therm Biol 37: 654-685. doi:10.1016/j.jtherbio.2012.08.004.
4. Gordon CJ, Becker P, Ali JS (1998) Behavioral thermoregulatory responses of single- and group-housed mice. Physiol Behav 65: 255-262. (Pubitemid 28548646)
5. Gaskill BN, Rohr SA, Pajor EA, Lucas JR, Garner JP (2009) Some like it hot: Mouse temperature preferences in laboratory housing. Appl Anim Behav Sci 116: 279-285.
6. Gaskill BN, Rohr SA, Pajor EA, Lucas JR, Garner JP (2011) Working with what you've got: Changes in thermal preference and behavior in mice with or without nesting material. J Therm Biol 36: 193-199. doi:10.1016/j.jtherbio.2011. 02.004.
7. Pearson OP (1947) The rate of metabolism of some small mammals. Ecology 28: 127-145.
8. Stanier MW (1975) Effect of body weight, ambient temperature and huddling on oxygen consumption and body temperature of young mice. Comp Biochem Physiol A Comp Physiol 51: 79-82.
9. Bryant DM, Hails CJ (1975) Mechanisms of heat conservation in the litters of mice (Mus musculus L.). Comp Biochem Physiol A Comp Physiol 50: 99-104.
10. Canals M, Rosenmann M, Novoa F, Bozinovic F (1998) Modulating factors of the energetic effectiveness of huddling in small mammals. Acta Theriolog 43: 337-348. (Pubitemid 29055428)
11. Vetulani T (1931) Untersuchungen über das Wachstum der Saugetiere in Abliangigkeit von der Anzahl zusammengehaltener Tiere. Biol generalis (Wien) 7: 71-98.
12. Retzlaff EG (1939) Studies in mass physiology: Growth rate with the white mouse. J Exper Zool 81: 343-356.
13. Prychodko W (1958) Effect of aggregation of laboratory mice (Mus musculus) on food intake at different temperatures. Ecology 39: 500-503.
14. Arakawa H, Blanchard D, Blanchard R (2007) Colony formation of C57BL/6J mice in visible burrow system: Identification of eusocial behaviors in a background strain for genetic animal models of autism. Behav Brain Res 176: 27-39. doi:10.1016/j.bbr.2006.07.027. (Pubitemid 44879622)
15. Gilbert C, McCafferty D, Le Maho Y, Martrette J-M, Giroud S, et al. (2010) One for all and all for one: The energetic benefits of huddling in endotherms. Biol Rev 85: 545-569. doi:10.1111/j.1469-185X.2009.00115.x.
16. Small WS (1899) Notes on the psychic development of the young white rat. Am J Psychol 11: 80-100.
17. Allee WC (1938) The social life of animals. 1st ed. W.W. Norton & Company, Inc.
18. Cairns RB, Nakelski JS (1971) On fighting in mice: Ontogenetic and experiential determinants. J Comp Physiol Psychol 74: 354-364. doi:10.1037/h0030584.
19. King JA, Connon H (1955) Effects of social relationships upon mortality in C57BL/10 mice. Physiol Zool 28: 233-239.
20. Phillips PK, Heath JE (1995) Dependency of surface temperature regulation on body size in terrestrial mammals. J Therm Biol 20: 281-289.
21. Blumberg MS (2001) The developmental context of thermal homeostasis. In: Blass EM, editor. Handbook of Behavioral Neurobiology, Vol. 13. New York: Kluwer Academic/Plenum, Vol. 13. 199-228.
22. Hull D (1973) Thermoregulation in young mammals. In: Whittow GC, editor. Comparative Physiology of Thermoregulation, Vol. 3 Special Aspects of Thermoregulation. New York, London: Academic Press, Vol. 3. 167-200.
23. Sayler A, Salmon M (1971) An ethological analysis of communal nursing by the house mouse (Mus musculus). Behaviour 40: 62-85.
24. Williams E, Scott J (1953) The development of social behavior patterns in the mouse, in relation to natural periods. Behaviour: 35-65.
25. Alberts JR (1978) Huddling by rat pups: Group behavioral mechanisms of temperature regulation and energy conservation. J Comp Physiol Psychol 92: 231.
26. Alberts JR (1978) Huddling by rat pups: Multisensory control of contact behavior. J Comp Physiol Psychol 92: 220-230.
27. Harshaw C, Alberts JR (2012) Group and individual regulation of physiology and behavior: A behavioral, thermographic, and acoustic study of mouse development. Physiol Behav 106: 670-682. doi:10.1016/j.physbeh.2012.05. 002.
28. Sokoloff G, Blumberg MS (2001) Competition and cooperation among huddling infant rats. Dev Psychobiol 39: 65-75.
29. Smith RE (1964) Thermoregulatory and Adaptive Behavior of Brown Adipose Tissue. Science 146: 1686-1689.
30. Girardier L (1983) Brown fat: an energy dissipating tissue. In: Girardier L, Stock MJ, editors. Mammalian Thermogenesis. London, New York: Springer. 50-98.
31. Ootsuka Y, de Menezes RC, Zaretsky DV, Alimoradian A, Hunt J, et al. (2009) Brown adipose tissue thermogenesis heats brain and body as part of the brain-coordinated ultradian basic rest-activity cycle. Neuroscience 164: 849-861. doi:10.1016/j.neuroscience.2009.08.013.
32. Sokoloff G, Blumberg MS, Adams MM (2000) A comparative analysis of huddling in infant Norway rats and Syrian golden hamsters: Does endothermy modulate behavior? Behav Neurosci 114: 585.
33. Alberts JR, Brunjes PC (1978) Ontogeny of thermal and olfactory determinants of huddling in the rat. J Comp Physiol Psychol 92: 897-906. (Pubitemid 9036048)
34. Alberts JR (2006) Huddling by rat pups: Ontogeny of individual and group behavior. Dev Psychobiol 49: 22-32. doi:10.1002/dev.20190.
35. Leonard CM (1974) Thermotaxis in golden hamster pups. J Comp Physiol Psychol 86: 458.
36. Johanson IB (1979) Thermotaxis in neonatal rat pups. Physiol Behav 23: 871-874.
37. Hoffman CM, Flory GS, Alberts JR (1999) Ontogenetic adaptation and learning: A developmental constraint in learning for a thermal reinforcer. Dev Psychobiol 34: 73-86. (Pubitemid 29120150)
38. Hoffman CM, Flory GS, Alberts JR (1999) Neonatal thermotaxis improves reversal of a thermally reinforced operant response. Dev Psychobiol 34: 87-99. (Pubitemid 29120151)
39. Sokoloff G, Blumberg MS, Boline EA, Johnson ED, Streeper NM (2002) Thermoregulatory behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus): Arousal, orientation, and locomotion. J Comp Psychol 116: 228-239. doi:10.1037//0735-7036.116.3.228.
40. Blumberg MS, Sokoloff G (1997) Dynamics of brown fat thermogenesis in week-old rats: Evidence of relative stability during moderate cold exposure. Physiol Zool 70: 324-330.
41. Sokoloff G, Blumberg MS (2002) Contributions of endothermy to huddling behavior in infant Norway rats (Rattus norvegicus) and Syrian golden hamsters (Mesocricetus auratus). J Comp Psychol 116: 240-246. doi:10.1037//0735-7036.116. 3.240.
42. Haig D (2008) Huddling: Brown fat, genomic imprinting and the warm inner glow. Curr Biol 18: R172-R174. doi:10.1016/j.cub.2007.12.040.
43. Quevedo S, Roca P, Picó C, Palou A (1998) Sex-associated differences in cold-induced UCP1 synthesis in rodent brown adipose tissue. Pflugers Arch 436: 689-695. (Pubitemid 28421366)
44. Valle A, García-Palmer FJ, Oliver J, Roca P (2007) Sex differences in brown adipose tissue thermogenic features during caloric restriction. Cell Physiol Biochem 19: 195-204. doi:10.1159/000099207.
45. Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, et al. (2002) Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem 277: 42958-42963. doi:10.1074/jbc.M207229200. (Pubitemid 35285674)
46. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, et al. (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360: 1509-1517. doi:10.1056/NEJMoa0810780.
47. Au-Yong ITH, Thorn N, Ganatra R, Perkins AC, Symonds ME (2009) Brown adipose tissue and seasonal variation in humans. Diabetes 58: 2583-2587. doi:10.2337/db09-0833.
48. Lynch CB, Sulzbach D, Connolly M (1988) Quantitative-genetic analysis of temperature regulation in Mus domesticus. IV. Pleiotropy and genotype-by-environment interactions. Am Nat 132: 521-537. (Pubitemid 19325421)
49. McDonald RB, Hamilton JS, Horwitz BA (1993) Influence of age and gender on brown adipose tissue norepinephrine turnover. Proc Soc Exp Biol Med 204: 117-121. (Pubitemid 23274064)
50. Rodríguez E, Monjo M, Rodriguez-Cuenca S, Pujol E, Amengual B, et al. (2001) Sexual dimorphism in the adrenergic control of rat brown adipose tissue response to overfeeding. Pflugers Arch 442: 396-403. (Pubitemid 32591982)
51. Valle A, Català-Niell A, Colom B, García-Palmer FJ, Oliver J, et al. (2005) Sex-related differences in energy balance in response to caloric restriction. Am J Physiol Endocrinol Metab 289: E15-E22. doi:10.1152/ajpendo.00553.2004. (Pubitemid 40874929)
52. Justo R, Frontera M, Pujol E, Rodriguez-Cuenca S, Lladó I, et al. (2005) Gender-related differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci 76: 1147-1158. doi:10.1016/j.lfs.2004.08.019. (Pubitemid 40037536)
53. Sack R, Gochberg-Sarver A, Rozovsky U, Kedmi M, Rosner S, et al. (2005) Lower core body temperature and attenuated nicotine-induced hypothermic response in mice lacking the b4 neuronal nicotinic acetylcholine receptor subunit. Brain Res Bull 66: 30-36. doi:10.1016/j.brainresbull.2005.02.032. (Pubitemid 40733109)
54. Gaskill BN, Gordon CJ, Pajor EA, Lucas JR, Davis JK, et al. (2013) Impact of nesting material on mouse body temperature and physiology. Physiol Behav 110-111: 87-95. doi:10.1016/j.physbeh.2012.12.018.
55. Hudson R, Bautista A, Reyes-Meza V, Montor JM, Rödel HG (2011) The effect of siblings on early development: A potential contributor to personality differences in mammals. Dev Psychobiol 53: 564-574. doi:10.1002/dev.20535.
56. Reyes-Meza V, Hudson R, Martínez-Gómez M, Nicolás L, Rödel HG, et al. (2011) Possible contribution of position in the litter huddle to long-term differences in behavioral style in the domestic rabbit. Physiol Behav 104: 778-785. doi:10.1016/j.physbeh.2011.07.019.
57. Bautista A, García-Torres E, Prager G, Hudson R, Rödel HG (2010) Development of behavior in the litter huddle in rat pups: Within- and between-litter differences. Dev Psychobiol 52: 35-43. doi:10.1002/dev.20409.
58. Granger CWJ (1969) Investigating causal relations by econometric models and cross-spectral methods. Econometrica 37: 424-438.
59. Granger CWJ (1988) Some recent development in a concept of causality. J Econom 39: 199-211.
60. Blumberg MS, Alberts JR (1990) Ultrasonic vocalizations by rat pups in the cold: An acoustic by-product of laryngeal braking? Behav Neurosci 104: 808-817. (Pubitemid 20365643)
61. Blumberg MS, Efimova IV, Alberts JR (1992) Thermogenesis during ultrasonic vocalization by rat pups isolated in a warm environment: A thermographic analysis. Dev Psychobiol 25: 497-510. doi:10.1002/dev.420250704.
62. Fisher RA (1950) The significance of deviations from expectation in a Poisson series. Biometrics 6: 17-24.
63. Sokal RR, Rohlf FJ (1981) Biometry: The principles and practice of statistics in biological research. New York: W H Freeman & Company.
64. 2-statistic. In Information Theory Proceedings (ISIT), 2012 IEEE International Symposium on (pp. 533-537). IEEE.
65. Granger CW (1980) Testing for causality: a personal viewpoint. J Econom Dyn Control 2: 329-352.
66. McPherson M, Smith-Lovin L, Cook JM (2001) Birds of a feather: Homophily in social networks. Annu Rev Sociol 27: 415-444.
67. Kerth G, König B (1999) Fission, fusion and nonrandom associations in female Bechstein's bats (Myotis bechsteinii). Behaviour 136: 1187-1202.
68. Broders HG, Forbes GJ (2004) Interspecific and intersexual variation in roostsite selection of northern long-eared and little brown bats in the Greater Fundy National Park ecosystem. J Wildl Manage 68: 602-610. (Pubitemid 39033516)
69. Johnson JS, Kropczynski JN, Lacki MJ, Langlois GD (2012) Social networks of Rafinesque's big-eared bats (Corynorhinus rafinesquii) in bottomland hardwood forests. J Mammal 93: 1545-1558. doi:10.1644/12-MAMM-A-097.1.
70. Ruckstuhl K (1998) Foraging behaviour and sexual segregation in bighorn sheep. Anim Behav 56: 99-106. doi:10.1006/anbe.1998.0745.
71. Conradt L (1998) Could asynchrony in activity between the sexes cause intersexual social segregation in ruminants? Proc R Soc Lond, B, Biol Sci 265: 1359-1363. doi:10.1098/rspb.1998.0442.
72. Haig D (2004) Genomic imprinting and kinship: How good is the evidence? Annu Rev Genet 38: 553-585. doi:10.1146/annurev.genet.37.110801.142741.
73. Haig D (2012) The strategic gene. Biol Philos 27: 461-479. doi:10.1007/s10539-012-9315-5.
74. Francis RC (1988) On the relationship between aggression and social dominance. Ethology 78: 223-237.
75. Scott JP, Fredericson E (1951) The causes of fighting in mice and rats. Physiol Zool 24: 273-309.
76. Crowcroft P, Rowe FP (1963) Social organisation and territorial behaviour of wild house mice. Proc Zool Soc Lond 140: 517-531.
77. Crowcroft P (1966) Mice all over. London: Foulis.
78. DeFries JC, McClearn GE (1970) Social dominance and Darwinian fitness in the laboratory mouse. Am Nat 104: 408-411.
79. Uhrich J (1938) The social hierarchy in albino mice. J Comp Psychol 25: 373.
80. Bevan W, Daves WF, Levy GW (1960) The relation of castration, androgen therapy and pre-test fighting experience to competitive aggression in male C57 BL/10 mice. Anim Behav 8: 6-12.
81. Mackintosh JH (1970) Territory formation by laboratory mice. Anim Behav 18: 177-183.
82. Poole TB, Morgan H (1976) Social and territorial behaviour of laboratory mice (Mus musculus L.) in small complex areas. Anim Behav 24: 476-480.
83. Gilbert C, McCafferty DJ, Giroud S, Ancel A, Blanc S (2012) Private heat for public warmth: How huddling shapes individual thermogenic responses of rabbit pups. PLoS ONE 7: e33553. doi:10.1371/journal.pone.0033553.t001.
84. Gilbert C, Blanc S, Giroud S, Trabalon M, Maho YL, et al. (2007) Role of huddling on the energetic of growth in a newborn altricial mammal. Am J Physiol-Reg I 293: R867-R876. doi:10.1152/ajpregu.00081.2007. (Pubitemid 47205074)
85. Branchi I (2009) The mouse communal nest: Investigating the epigenetic influences of the early social environment on brain and behavior development. Neurosci Biobehav Rev 33: 551-559. doi:10.1016/j.neubiorev.2008.03.011.
86. Hayes JP, Speakman JR, Racey PA (1992) The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis). Physiol Zool: 742-762. (Pubitemid 24410981)
87. Bond TL, Neumann PE, Mathieson WB, Brown RE (2002) Nest building in nulligravid, primigravid and primiparous C57BL/6J and DBA/2J mice (Mus musculus). Physiol Behav 75: 551-555. (Pubitemid 34327962)
88. Brown RE, Mathieson WB, Stapleton J, Neumann PE (1999) Maternal behavior in female C57BL/6J and DBA/2J inbred mice. Physiol Behav 67: 599-605. (Pubitemid 29488540)
89. Champagne FA, Curley JP, Keverne EB, Bateson PPG (2007) Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav 91: 325-334. doi:10.1016/j.physbeh.2007.03.014. (Pubitemid 46795437)
90. Barnett SA (1956) Endothermy and ectothermy in mice at -3 C. J Exp Biol 33: 124-133.
91. Sales GD, Skinner NC (1979) The effect of ambient temperature on body temperature and on ultrasonic behaviour in litters of albino laboratory mice deprived of their mothers. J Zool 187: 265-281.
92. Meyer P (2010) Maternal behavior of C57BL/6 mice with oxytocin-disrupted offspring Indiana University.
93. Rödel HG, Bautista A, García-Torres E, Martínez- Gómez M, Hudson R (2008) Why do heavy littermates grow better than lighter ones? A study in wild and domestic European rabbits. Physiol Behav 95: 441-448. doi:10.1016/j.physbeh.2008.07.011.
94. Dimitsantos E, Escorihuela RM, Fuentes S, Armario A, Nadal R (2007) Litter size affects emotionality in adult male rats. Physiol Behav 92: 708-716. doi:10.1016/j.physbeh.2007.05.066. (Pubitemid 350016132)
95. Rödel HG, Holst von D (2009) Features of the early juvenile development predict competitive performance in male European rabbits. Physiol Behav 97: 495-502. doi:10.1016/j.physbeh.2009.04.005.
96. D'Eath RB, Lawrence AB (2004) Early life predictors of the development of aggressive behaviour in the domestic pig. Anim Behav 67: 501-509. doi:10.1016/j.anbehav.2003.06.010.
97. Ryan BC, Vandenbergh JG (2002) Intrauterine position effects. Neurosci Biobehav Rev 26: 665-678. (Pubitemid 35477574)
98. Saal vom FS (1989) Sexual differentiation in litter-bearing mammals: influence of sex of adjacent fetuses in utero. J Anim Sci 67: 1824-1840.
99. de Medeiros CB, Rees SL, Llinas M, Fleming AS, Crews D (2010) Deconstructing early life experiences: Distinguishing the contributions of prenatal and postnatal factors to adult male sexual behavior in the rat. Psychol Sci 21: 1494-1501. doi:10.1177/0956797610382122.
100. Crews D (2011) Epigenetic modifications of brain and behavior: Theory and practice. Horm Behav 59: 393-398. doi:10.1016/j.yhbeh.2010.07.001.
101. Fairless AH, Dow HC, Kreibich AS, Torre M, Kuruvilla M, et al. (2012) Sociability and brain development in BALB/cJ and C57BL/6J mice. Behav Brain Res 228: 299-310. doi:10.1016/j.bbr.2011.12.001.
102. Rodríguez AM, Monjo M, Roca P, Palou A (2002) Opposite actions of testosterone and progesterone on UCP1 mRNA expression in cultured brown adipocytes. Cell Mol Life Sci 59: 1714-1723. (Pubitemid 35346975)
103. Monjo M, Rodríguez AM, Palou A, Roca P (2003) Direct effects of testosterone, 17 beta-estradiol, and progesterone on adrenergic regulation in cultured brown adipocytes: potential mechanism for gender-dependent thermogenesis. Endocrinology 144: 4923-4930. doi:10.1210/en.2003-0537. (Pubitemid 37378406)
104. Lisk RD (1971) Oestrogen and progesterone synergism and elicitation of maternal nest-building in the mouse (Mus musculus). Anim Behav 19: 606-610.
105. Lisk RD, Russell JA, Kahler SG, Hanks JB (1973) Regulation of hormonally mediated maternal nest structure in the mouse (Mus musculus) as a function of neonatal hormone manipulation. Anim Behav 21: 296-301.