Lactational programming? Mother's milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta)

American Journal of Primatology

Volumn 72, Issue 6, 2010, Pages 522-529

  Hinde, Katie ^a,b   Capitanio, John P ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Behavioral syndromes; Infant development; Lactation; Nutritional programming; Personality

Indexed keywords

BEHAVIORAL RESPONSE; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL CONDITIONS; LACTATION; MILK; PRIMATE;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; CHEMISTRY; ENERGY METABOLISM; FEMALE; LACTATION; MACACA; MALE; METABOLISM; MILK; NUTRITIONAL STATUS; NUTRITIONAL VALUE; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; SUCKLING; TEMPERAMENT;

ANIMALS; ANIMALS, SUCKLING; BEHAVIOR, ANIMAL; ENERGY METABOLISM; FEMALE; LACTATION; MACACA MULATTA; MALE; MILK; NUTRITIONAL STATUS; NUTRITIVE VALUE; TEMPERAMENT;

MACACA; MACACA MULATTA; MAMMALIA;

EID: 77951693882     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20806     Document Type: Article

References (64)

1. Akers RM. 2002. Lactation and the mammary gland. Iowa: Blackwell Publishing.
2. Andrews MW, Rosenblum LA. 1994. The development of affiliative and agonistic social patterns in differentially reared monkey. Child Development 65:1398-1404.
3. Andrews MW, Sunderland G, Rosenblum LA. 1993. Impact of foraging demand on conflict within mother-infant dyads. In: Mason WA, Mendoza SP, editors. Primate social conflict. Albany: SUNY Press. p 229-252.
4. Armitage JA, Khan IY, Taylor PD, Nathanielz PW, Poston L. 2004. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals. The Journal of Physiology 561:355-377.
5. Barker DJP, Eriksson JG, Forsen T, Osmond C. 2002. Fetal origins of adult disease: strength of effects and biological basis. International Journal of Epidemiology 31:1235-1239.
6. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, Gluckman P, Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE. 2004. Developmental plasticity and human health. Nature 430:419-421.
7. Bentley GR. 1999. Aping our ancestors: comparative aspects of reproductive ecology. Evolutionary Anthropology 7:175-185.
8. Bercovich FB, Harvey NC. 2004. Reproductive life history. In: Thierry B, Singh M, Kaumanns W, editors. Macaque societies: a model for the study of social organization. New York: Cambridge University Press. p 61-80.
9. Bercovitch FB, Lebron MR, Martinez HS, Kessler MJ. 1998. Primigravidity, body weight, and costs of rearing first offspring in rhesus macaques. American Journal of Prima-tology 46:135-144.
10. Capitanio JP, Rasmussen KLR, Snyder DS, Laudenslager M, Reite M. 1986. Long-term follow-up of previously separated pigtail macaques: group and individual differences in response to novel situations. Journal of Child Psychology and Psychiatry 27:531-538.
11. Capitanio JP, Mendoza SP, Mason WA, Maninger N. 2005. Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Developmental Psychobiology 46:318-330.
12. Capitanio JP, Mason WA, Mendoza SP, Del Rosso L, Roberts JA. 2006. Nursery rearing and biobehavioral organization. In: Sackett GP, Ruppenthal GC, Elias K, editors. Nursery rearing of nonhuman primates in the 21st century. New York: Springer. p 191-214.
13. Champagne FA, Francis DD, Mar A, Meaney MJ. 2003. Variations in maternal care in the rat as mediating influence of the effects of environment on development. Physiology & Behavior 79:359-371.
14. Cheney DL, Seyfarth RM, Fischer J, Beehner JC, Bergman TJ, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB. 2006. Reproduction, mortality, and female reproductive success in chacma baboons of the Okavango Delta, Botswana. In: Swedell L, Leigh SR, editors. Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives. New York: Springer. p 147-176.
15. Debyser IWJ. 1995. Platyrrhine juvenile mortality in captivity and in the wild. International Journal of Primatology 16:909-933.
16. Desai M, Hales CN. 1997. Role of fetal and infant growth in programming metabolism in later life. Biological Reviews 72:329-348.
17. Dewitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 13:77-81.
18. Fairbanks LA. 1996. Individual differences in maternal style: causes and consequences for mothers and offspring. Advances in the Study of Behavior 25:579-611.
19. Fairbanks LA. 2000. The developmental timing of primate play: a neural selection model. In: Parker ST, Langer S, McKinney ML, editors. Biology, brains, and behavior. Oxford: James Currey, Inc. p 131-158.
20. Fish EW, Shahrokh D, Bagot R, Caldji C, Bredy T, Szyf M, Meaney MJ. 2004. Epigenetic programming of stress responses through variations in maternal care. Annals of the New York Academy of Sciences 1036:167-180.
21. Fraser AM, Brockert JE, Ward RH. 1995. Association of young maternal age with adverse reproductive outcomes. The New England Journal of Medicine 332:1113-1117.
22. Golub MS, Hogrefe CE, Germann SL. 2007. Iron deprivation during fetal development changes the behavior of juvenile rhesus monkeys. The Journal of Nutrition 137:979-984.
23. Golub MS, Hogrefe CE, Widaman KF, Capitanio JP. 2009. Iron deficiency anemia and affective response in rhesus monkey infants. Developmental Psychobiology 51:47-59.
24. Gomez JA, Landete-Castillejos T, Garcia AJ, Gallego L. 2002. Effect of calving advance on milk production and composition, and calf growth in Iberian deer (Cervus elaphus hispanicus). Small Ruminant Research 44:213-218.
25. Hinde K. 2007a. Milk composition varies in relation to the presence and abundance of Balantidium coli in the mother in captive rhesus macaques (Macaca mulatta). American Journal of Primatology 69:625-634.
26. Hinde K. 2007b. First-time macaque mothers bias milk composition in favor of sons. Current Biology 17:R958-R959.
27. Hinde K. 2009. Richer milk for sons but more milk for daughters: sex biased investment during lactation varies with maternal life history in rhesus macaques. American Journal of Human Biology 21:512-519.
28. Hinde K, Power ML, Oftedal OT. 2009. Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation. American Journal of Physical Anthropology 138:148-157.
29. Jacobs B, Chugan HT, Allad V, Chen S, Phelps ME, Pollack DB, Raleigh MJ. 1995. Developmental changes in brain metabolism in rhesus macaques and vervet monkeys revealed by positron emission tomography. Cerebral Cortex 5:222-233.
30. Kuzawa C. 2007. Developmental origins of life history: growth, productivity, and reproduction. American Journal of Human Biology 19:654-661.
31. Landete-Castillejos T, Garcia A, Gallego G. 2001. Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effects of birth date and hind milk production and composition. Journal of Animal Science 79:1085-1092.
32. Lavenex P, Lavanex PB, Amaral DG. 2007. Postnatal development of the primate hippocampal formation. Developmental Neuroscience 29:179-192.
33. Lawlis GF, Liu E. 1972. Judgement of counseling process: Reliability, agreement, and error. Psychological Bulletin 78:17-20.
34. Lummaa V, Clutton-Brock T. 2001. Early development, survival, and reproduction in humans. Trends in Ecology & Evolution 17:141-147.
35. Maestripieri D. 2009. Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM, editors. Maternal effects in mammals. Chicago: The University of Chicago Press.
36. Mellish JE, Iverson SJ, Bowen WD. 1999. Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiological and Biochemical Zoology 72:67-69.
37. Metcalfe NB, Monaghan P. 2001. Compensation for a bad start: grow now and pay later? Trends in Ecology & Evolution 16:254-260.
38. Mosseau TA, Fox CW. 1998. The adaptive significance of maternal effects. Trends in Ecology & Evolution 13:403-407.
39. Muthen LK, Muthen BO. 1998-2001. Mplus user's guide, 2nd ed. Los Angeles, CA: Muthen & Muthen.
40. Oftedal OT. 1984. Milk composition, milk yield and energy output at peak lactation: a comparative review. Zoological Society of London 51:33-85.
41. Oftedal OT, Iverson SJ. 1995. Comparative analysis of non-human primate milks. In: Jenson RG, editor. Handbook of milk composition. San Diego: Academic Press. p 749-789.
42. Oftedal OT, Bowen WD, Boness DJ. 1993. Energy transfer by lactating hooded seals and nutrient deposition in their pups during the four days from birth to weaning. Physiological Zoology 66:412-436.
43. Oftedal OT, Bowen WD, Boness DJ. 1996. Lactation performance and nutrient deposition in pups of the harp seal (Phoca groenlandica) on ice floes off southeast Labrador. Physiological Zoology 69:635-657.
44. Ota K, Makino Y, Kimura M. 1991. Lactation in the Japanese monkey (Macaca fuscata): yield and composition of milk and nipple preference of young. Primates 32:35-48.
45. Rahmanifar A, Kirksey A, Wachs TD, McCabe GP, Bishry Z, Galal OM, Harrison GG, Jerome NW. 1993. Diet during lactation associated with infant behavior and caregiverinfant interaction in a semirural Egyptian village. Journal of Nutrition 123:164-175.
46. Räsänen K, Kruuk LEB. 2007. Maternal effects and evolution at ecological time-scales. Functional Ecology 21:408-421.
47. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007. Integrating animal temperament within ecology and evolution. Biological Reviews 82:291-318.
48. Richard AF, Goldstein SJ, Dewar RE. 1989. Weed macaques: the evolutionary implications of macaque feeding ecology. International Journal of Primatology 10:569-594.
49. Riek A. 2008. Relationship between milk energy intake and growth rate in suckling mammalian young at peak lactation: an updated meta-analysis. Journal of Zoology 274:160-170.
50. Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD. 2006. Age-related patterns of reproductive success among female mountain gorillas. American Journal of Physical Anthro-pology 131:511-521.
51. Roberts SB, Cole TJ, Coward WA. 1985. Lactational performance in relation to energy intake in the baboon. American Journal of Clinical Nutrition 41:1270-1276.
52. Rosenblum LA, Forger C, Noland S, Trost RC, Coplan JD. 2001. Response of adolescent bonnet macaques to an acute fear stimulus as a function of early rearing conditions. Developmental Psychobiology 39:40-45.
53. Smith BR, Blumstein DT. 2008. Fitness consequences of personality: a meta-analysis. Behavioral Ecology 19: 448-455.
54. Suomi SJ, Ripp C. 1983. A history of motherless mother monkey mothering at the University of Wisconsin Primate Laboratory. In: Reite M, Caine N, editors. Child abuse: The Nonhuman Primate Data. New York: Liss. p 49-78.
55. Szyf M, Weaver I, Meaney M. 2007. Maternal care, the epigenome, and phenotypic differences in behavior. Reproductive Toxicology 24:9-19.
56. Tardif SD, Power ML, Oftedal OT, Power RA, Layne DG. 2001. Lactation, maternal behavior and infant growth in common marmoset monkeys (Callithrix jacchus): effects of maternal size and litter size. Behavioral Ecology and Sociobiology 51:17-25.
57. Tinsley HEA, Weiss DJ. 1975. Interrater reliability and agreement of subjective judgements. Journal of Counseling Psychology 22:358-376.
58. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ. 2004. Epigenetic programming by maternal behavior. Nature Neuroscience 7:847-854.
59. Weinstein TAR, Capitanio JP. 2008. Individual differences in infant temperament predict social relationships of yearling rhesus monkeys, Macaca mulatta. Animal Behavior 76:455-465.
60. Weinstein TAR, Capitanio JP, Gosling SD. 2008. Personality in animals. In: John OP, Robinns RW, Pervin LA, editors. Handbook of personality: theory and research, 3rd ed. New York: Guilford Press. p 328-348.
61. Wells JCK. 2007. The thrifty phenotype as an adaptive maternal effect. Biological Reviews 82:143-172.
62. West-Eberhard MJ. 2003. Developmental plasticity and evolution. Oxford: Oxford University Press.
63. Wolf M, Sander van Doorn G, Leimar O, Weissing FJ. 2007. Life-history tradeoffs favor the evolution of animal personalities. Nature 447:581-584.
64. Zecevic N, Bourgeois JP, Rakic P. 1989. Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Brain Research 50:11-32.