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Lactational Programming of Infant Behavioral Phenotype

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Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR,volume 37))

Abstract

The goal of the present chapter is to familiarize the reader with the limited body of knowledge on mother’s milk and infant behavior and thereby motivate future investigations on the complex inter-relationships among early nutrition, neurodevelopment, and behavioral phenotype. After briefly summarizing what is known about mother’s milk and infant growth, I will provide a conceptual framework for “behavioral phenotype” and discuss attributes of mother’s milk that have been associated with infant behavioral phenotype. To date, this has only been directly studied in rodents and rhesus macaques, and glucocorticoids in milk have received the greatest research effort. I will then explore the potential proximate mechanisms by which cortisol and other milk attributes mediate metabolic and neurobiological development and thereby influence infant behavior.

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Notes

  1. 1.

    Energy balance reflects the ratio of energy intake vs. energy expenditure. When these are equal, an individual is in neutral energy balance and is neither gaining nor losing body mass. Negative energy balance is when an individual’s energy expenditure exceeds energy intake, requiring the mobilization of body reserves for somatic maintenance and body mass decreases. Positive energy balance occurs when energy intake exceeds energy expenditure and individuals are gaining mass.

  2. 2.

    When describing published studies in detail, I will use the same terms used by the investigators conducting the research. Elsewhere I will primarily use “behavioral phenotype,” the most inclusive term for individual behavior.

References

  • Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82

    PubMed  CAS  Google Scholar 

  • Akers RM (2002) Lactation and the mammary gland. Iowa State Press

    Google Scholar 

  • Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Animal Behaviour 65:821–840

    Google Scholar 

  • Alpers DH (2010) Nutrient sensing in the gastrointestinal tract. Curr Opin Gastroenterol 26(2):134–139

    PubMed  Google Scholar 

  • Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge

    Google Scholar 

  • Andrews MW, Rosenblum LA (1994) The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Dev 65(5):1398–1404

    PubMed  CAS  Google Scholar 

  • Andrews MW, Sunderland G, Rosenblum LA (1993) Impact of foraging demand on conflict within mother-infant dyads. In: Mason WA, Mendoza SP (eds) Primate social conflict. SUNY Press, Albany, pp 229–252

    Google Scholar 

  • Angelucci L, Patacchioli FR, Chierichetti C, Laureti S (1983) Perinatal mother-offspring pituitary-adrenal interrelationship in rats: corticosterone in milk may affect adult life. Endocrinol Exp 17(3–4):191–205

    PubMed  CAS  Google Scholar 

  • Angelucci L, Patacchioli FR, Scaccianoce S, Di Sciullo A, Cardillo A, Maccari S (1985) A model for later-life effects of perinatal drug exposure: maternal hormone mediation. Neurobehav Toxicol Teratol 7(5):511–517

    PubMed  CAS  Google Scholar 

  • Arnould JPY, Hindell MA (2002) Milk consumption, body composition and pre-weaning growth rates of Australian fur seal (Arctocephalus pusillus doriferus) pups. J Zool 256:351–359

    Google Scholar 

  • Arnould JPY, Ramsay MA (1994) Milk production and milk consumption in polar bears during the ice-free period in western Hudson Bay. Can J Zool 72(8):1365–1370

    Google Scholar 

  • Averette LA, Odle J, Monaco MH, Donovan SM (1999) Dietary fat during pregnancy and lactation increases milk fat and insulin-like growth factor I concentrations and improves neonatal growth rates in swine. J Nutr 129(12):2123–2129

    PubMed  CAS  Google Scholar 

  • Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M (2011) Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 25(3):397–407

    PubMed  CAS  Google Scholar 

  • Barrett KE, Barman SM, Boitano S, Brooks H (2010) Chapter 21. Endocrine functions of the pancreas & regulation of carbohydrate metabolism. In: Barrett KE, Barman SM, Boitano S, Brooks H (eds) Ganong’s review of medical physiology, 23e. http://www.accessmedicine.com/content.aspx?aID=5241979. Retrieved 12 Mar 2012

  • Beecher MD (2007) Signalling systems for individual recognition: an information theory approach. J Econ Behav Organ 63:193–206

    Google Scholar 

  • Bergmüller R, Schürch R, Hamilton IM (2010) Evolutionary causes and consequences of consistent individual variation in cooperative behaviour. Philos Trans R Soc Lond B Biol Sci 365(1553):2751–2764

    PubMed  Google Scholar 

  • Bergvall UA, Schäpers A, Kjellander P, Weiss A (2011) Personality and foraging decisions in fallow deer, Dama dama. Animal Behaviour 81:101–112

    Google Scholar 

  • Biro PA, Stamps JA (2010) Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol 25(11):653–659

    PubMed  Google Scholar 

  • Blum D (2004) Love at Goon Park: Harry Harlow and the science of affection. Berkley Books, New York

    Google Scholar 

  • Blumstein DT, Patton ML, Saltzman W (2006) Faecal glucocorticoid metabolites and alarm calling in free-living yellow-bellied marmots. Biol Let 2(1):29–32

    CAS  Google Scholar 

  • Bock J, Johnson SE (2004) Subsistence ecology and play among the Okavango delta peoples of Botswana. Human Nature 15:63–81

    Google Scholar 

  • Boesch C, Kohou G, Néné H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Taï forest. Am J Phys Anthropol 130(1):103–115

    PubMed  Google Scholar 

  • Both C, Dingmanse NJ, Drent PJ, Tinbergen JM (2005) Pairs of extreme avian personalities have highest reproductive success. J Anim Ecol 74:667–674

    Google Scholar 

  • Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N, Boesch C, Vigilant L (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci 102(26):9418–9423

    PubMed  CAS  Google Scholar 

  • Broberger C (2005) Brain regulation of food intake and appetite: molecules and networks. J Intern Med 258(4):301–327

    PubMed  CAS  Google Scholar 

  • Bunge M (1985) From mindless neuroscience and brainless psychology to neuropsychology. Ann Theoretical Psychol 3:115–133

    Google Scholar 

  • Butte NF, Garza C, Stuff JE, O’Brian Smith E, Nichols BL (1984) Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr 39:296–306

    PubMed  CAS  Google Scholar 

  • Cameron JL (1996) Regulation of reproductive hormone secretion in primates by short-term changes in nutrition. Rev Reprod 1(2):117–126

    PubMed  CAS  Google Scholar 

  • Capitanio JP, Mendoza SP, Mason WA, Maninger N (2005) Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Dev Psychobiol 46:318–330

    PubMed  CAS  Google Scholar 

  • Capitanio JP, Abel K, Mendoza SP, Blozis SA, McChesney MB, Cole SW, Mason WA (2008) Personality and serotonin transporter genotype interact with social context to affect immunity and viral set-point in simian immunodeficiency virus disease. Brain Behav Immun 22(5):676–689

    PubMed  CAS  Google Scholar 

  • Careau V, Réale D, Humphries MM, Thomas DW (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. Am Nat 175(6):753–758

    PubMed  Google Scholar 

  • Casolini P, Cigliana G, Alemà GS, Ruggieri V, Angelucci L, Catalani A (1997) Effect of increased maternal corticosterone during lactation on hippocampal corticosteroid receptors, stress response and learning in offspring in the early stages of life. Neuroscience 79(4):1005–1012

    PubMed  CAS  Google Scholar 

  • Catalani A, Marinelli M, Scaccianoce S, Nicolai R, Muscolo LA, Porcu A, Korányi L, Piazza PV, Angelucci L (1993) Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance. Brain Res 624:209–215

    PubMed  CAS  Google Scholar 

  • Catalani A, Casolini P, Scaccianoce S, Patacchioli FR, Spinozzi P, Angelucci L (2000) Maternal corticosterone during lactation permanently affects brain corticosteroid receptors, stress response and behaviour in rat progeny. Neuroscience 100(2):319–325

    PubMed  CAS  Google Scholar 

  • Catalani A, Casolini P, Cigliana G, Scaccianoce S, Consoli C, Cinque C, Zuena AR, Angelucci L (2002) Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharmacol Biochem Behav 73(1):105–114

    PubMed  CAS  Google Scholar 

  • Chilliard Y, Delavaud C, Bonnet M (2005) Leptin expression in ruminants: nutritional and physiological regulations in relation with energy metabolism. Domest Anim Endocrinol 29(1):3–22

    PubMed  CAS  Google Scholar 

  • Cohen S, Doyle WJ, Turner R, Alper CM, Skoner DP (2003) Sociability and susceptibility to the common cold. Psychol Sci 14(5):389–395

    PubMed  Google Scholar 

  • Coplan JD, Smith EL, Altemus M, Mathew SJ, Perera T, Kral JG, Gorman JM, Owens MJ, Nemeroff CB, Rosenblum LA (2006) Maternal-infant response to variable foraging demand in nonhuman primates: effects of timing of stressor on cerebrospinal fluid corticotropin-releasing factor and circulating glucocorticoid concentrations. Ann N Y Acad Sci 1071:525–533

    PubMed  CAS  Google Scholar 

  • Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Animal Behaviour 41:1045–1056

    Google Scholar 

  • Dauncey MJ (1990) Activity and energy expenditure. Can J Physiol Pharmacol 68:17–27

    PubMed  CAS  Google Scholar 

  • De Ruiter JR, Van Hooff JARAM, Scheffrahn W (1994) Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129:203–224

    Google Scholar 

  • Del Prado M, Delgado G, Villalpando S (1997) Maternal lipid intake during pregnancy and lactation alters milk composition and production and litter growth in rats. J Nutr 127(3):458–462

    PubMed  Google Scholar 

  • Dingemanse NJ, Wolf M (2010) Recent models for adaptive personality differences: a review. Philos Trans R Soc Lond B Biol Sci 365(1560):3947–3958

    PubMed  Google Scholar 

  • Djurhuus CB, Gravholt CH, Nielsen S, Pedersen SB, Møller N, Schmitz O (2004) Additive effects of cortisol and growth hormone on regional and systemic lipolysis in humans. Am J Physiol Endocrinol Metab 286(3):E488–E494

    PubMed  CAS  Google Scholar 

  • Dochtermann NA, Roff DA (2010) Applying a quantitative genetics framework to behavioural syndrome research. Philos Trans R Soc Lond B Biol Sci 365(1560):4013–4020

    PubMed  Google Scholar 

  • El-Masry KA, Marai IFM (1991) Comparison between Friesians and water buffaloes in growth rate, milk production and some blood constituents, during winter and summer conditions of Egypt. Animal Production 53:39–43

    Google Scholar 

  • Fairbanks LA (1996) Individual differences in maternal style: causes and consequences for mothers and infants. Adv Study Behav 25:579–611

    Google Scholar 

  • Fairbanks LA (2000) The developmental timing of primate play: a neural selection model. In: Parker ST, Langer S, McKinney ML (eds) Biology, brains, and behavior. James Currey Inc, Oxford, pp 131–158

    Google Scholar 

  • Fairbanks LA (2001) Individual differences in response to a stranger: social impulsivity as a dimension of temperament in vervet monkeys (Cercopithecus aethiops sabaeus). J Comp Psychol 115:22–28

    PubMed  CAS  Google Scholar 

  • Fairbanks LA, Hinde K (2012) Behavioral response of mothers and infants to variation in maternal condition: adaptation, compensation and resilience. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Fairbanks L, Jorgensen M, Huff A, Blau K, Hung YY, Mann JJ (2004) Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys. Am J Primatol 64:1–17

    PubMed  Google Scholar 

  • 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. Ann N Y Acad Sci 1036:167–180

    PubMed  Google Scholar 

  • Forsythe P, Sudo N, Dinan T, Taylor VH, Bienenstock J (2010) Mood and gut feelings. Brain Behav Immun 24(1):9–16

    PubMed  Google Scholar 

  • Glynn LM, Davis EP, Schetter CD, Chicz-Demet A, Hobel CJ, Sandman CA (2007) Postnatal maternal cortisol levels predict temperament in healthy breastfed infants. Early Hum Dev 83(10):675–681

    PubMed  CAS  Google Scholar 

  • Golub MS, Hogrefe CE, Widaman KF, Capitanio JP (2009) Iron deficiency anemia and affective response in rhesus monkey infants. Dev Psychobio 51:47–59

    CAS  Google Scholar 

  • Gosling SD (2001) From mice to men: what can we learn about personality from animal research? Psychol Bull 127:45–86

    PubMed  CAS  Google Scholar 

  • Groothuis, Trillmich (2011) Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol 53:641–655

    PubMed  Google Scholar 

  • Hinde K (2007) First-time macaque mothers bias milk composition in favor of sons. Curr Biol 17:R958–R959

    PubMed  CAS  Google Scholar 

  • Hinde K (2009) Richer milk for sons but more milk for daughters: sex bias investment during lactation varies with maternal life history in rhesus macaques. Am J Hum Biol 21:512–519

    PubMed  Google Scholar 

  • Hinde K, Capitanio JP (2010) Lactational programming? Mother’s milk predicts infant temperament and behavior. Am J Primatol 72:522–529

    PubMed  Google Scholar 

  • Hinde K, Milligan LM (2011) Primate milk synthesis: proximate mechanisms and ultimate perspectives. Evol Anthropol 20:9–23

    PubMed  Google Scholar 

  • Hinde K, Power ML, Oftedal LT (2009) Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation. Am J Phys Anthropol 138:148–157

    PubMed  Google Scholar 

  • Hindell MA, Bryden MM, Burton HR (1994) Early growth and milk-composition in southern elephant seals (Mirounga leonina). Aust J Zool 42(6):723–732

    Google Scholar 

  • Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, Le Bouc Y, Deal CL, Lillycrop K, Scharfmann R, Sheppard A, Skinner M, Szyf M, Waterland RA, Waxman DJ, Whitelaw E, Ong K, Albertsson-Wikland K (2011) Child health, developmental plasticity, and epigenetic programming. Endocr Rev 32(2):159–224

    PubMed  CAS  Google Scholar 

  • Honess PE, Marin CM (2006) Behavioural and physiological aspects of stress and aggression in nonhuman primates. Neurosci Biobehav Rev 30(3):390–412

    PubMed  CAS  Google Scholar 

  • Houston AI (2010) Evolutionary models of metabolism, behaviour and personality. Philos Trans R Soc Lond B Biol Sci 365(1560):3969–3975

    PubMed  Google Scholar 

  • Iverson SJ, BowenWD BDJ, Oftedal OT (1993) The effect of maternal size and milk energy output on pup growth in grey seals (Halichoerus grypus). Physiol Zool 66:61–88

    Google Scholar 

  • Jaman MJ, Huffman MA (2008) Enclosure environment affects the activity budgets of captive Japanese macaques (Macaca fuscata). Am J Primatol 12:1133–1144

    Google Scholar 

  • Johnson HG, Ekman P, Friesen W (1976) A behavioral phenotype in the de Lange syndrome. Pediatr Res 10:843–850

    PubMed  CAS  Google Scholar 

  • Johnston RE, Peng A (2008) Memory for individuals: hamsters (Mesocricetus auratus) require contact to develop multicomponent representations (concepts) of others. J Comp Psychol 122(2):121–131

    PubMed  Google Scholar 

  • Jones KA, Godin JG (2010) Are fast explorers slow reactors? Linking personality type and anti-predator behaviour. Proc Biol Sci 277(1681):625–632

    PubMed  Google Scholar 

  • Kandel ER, Squire LR (2000) Neuroscience: breaking down scientific barriers to the study of brain and mind. Science 290(5494):1113–1120

    PubMed  CAS  Google Scholar 

  • Kappeler PM, Port M (2008) Mutual tolerance or reproductive competition? Patterns of reproductive skew among male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 62: 1477–1488

    Google Scholar 

  • Kappeler PM, Schäffler L (2008) The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol 62:1007–1015

    Google Scholar 

  • Khani S, Tayek JA (2001) Cortisol increases gluconeogenesis in humans: its role in the metabolic syndrome. Clin Sci (Lond) 101(6):739–747

    CAS  Google Scholar 

  • Kinnally E (2012) Genome-environment coordination in neurobehavioral development. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Kinnally EL, Jensen HA, Ewing JH, French JA (2006) Serotonin function is associated with behavioral response to a novel conspecific in marmosets. Am J Primatol 68:812–824

    PubMed  CAS  Google Scholar 

  • Kondoh T, Mallick HN, Torii K (2009) Activation of the gut-brain axis by dietary glutamate and physiologic significance in energy homeostasis. Am J Clin Nutr 90(3):832S–837S

    PubMed  CAS  Google Scholar 

  • Koolhaas JM, de Boer SF, Coppens CM, Buwalda B (2010) Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol 31:307–321

    PubMed  CAS  Google Scholar 

  • Kurvers RH, Prins HH, van Wieren SE, van Oers K, Nolet BA, Ydenberg RC (2010) The effect of personality on social foraging: shy barnacle geese scrounge more. Proc Biol Sci 277(1681): 601–608

    PubMed  Google Scholar 

  • Landete-Castillejos T, Garcia A, Gallego L (2001) Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effects of birth date and hind milk production and composition. J Anim Sci 79(5):1085–1092

    PubMed  CAS  Google Scholar 

  • Langer P (2003) Lactation, weaning period, food quality, and digestive tract differentiations in eutheria. Evolution 57:1196–1215

    PubMed  Google Scholar 

  • Langer P (2008) The phases of maternal investment in eutherian mammals. Zool 111:148–162

    Google Scholar 

  • Li Z, Rogers E (2004) Habitat quality and activity budgets of white-headed langurs in Fusui. China Inter J Primatol 25:41–54

    Google Scholar 

  • Lydersen C, Hammill MO, Kovacs KM (1995) Milk intake, growth and energy consumption in pups of ice-breeding grey seals (Halichoerus grypus) from the Gulf of St. Lawrence, Canada. J Comp Physiol B 164(8):585–592

    PubMed  CAS  Google Scholar 

  • Machado CJ (2012) Maternal influences on social and neural development in rhesus monkeys. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Maestripieri D (2009) Maternal influenced on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University Chicago Press, Chicago, pp 256–291

    Google Scholar 

  • Manuck SB, Kaplan JR, Rymeski BA, Fairbanks LA, Wilson ME (2003) Approach to a social stranger is associated with low central nervous system serotonergic responsivity in female cynomolgus monkeys (Macaca fascicularis). Am J Primatol 61:187–194

    PubMed  CAS  Google Scholar 

  • Margetic S, Gazzola C, Pegg GG, Hill RA (2002) Leptin: a review of its peripheral actions and interactions. Int J Obes Relat Metab Disord 26(11):1407–1433

    PubMed  CAS  Google Scholar 

  • Martin M, Sela D (2012) Infant gut microbiota: developmental influences and health outcomes? In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Meerlo P, Horvath KM, Luiten PG, Angelucci L, Catalani A, Koolhaas JM (2001) Increased maternal corticosterone levels in rats: effects on brain 5-HT1A receptors and behavioral coping with stress in adult offspring. Behav Neurosci 115(5):1111–1117

    PubMed  CAS  Google Scholar 

  • Mellish JA, Iverson SJ, Don BW (1999) Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics. Physiol Biochem Zool 72(6):677–690

    PubMed  CAS  Google Scholar 

  • Milligan LA (2012) Do bigger brains mean better milk? In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Munks SA, Green B (1997) Milk consumption and growth in a marsupial arboreal folivore, the common ringtail possum, Pseudocheirus peregrinus. Physiol Zool 70(6):691–700

    PubMed  CAS  Google Scholar 

  • Murphy KG, Dhillo WS, Bloom SR (2006) Gut peptides in the regulation of food intake and energy homeostasis. Endocr Rev 27(7):719–727

    PubMed  CAS  Google Scholar 

  • Näslund E, Hellström PM (2007) Appetite signaling: from gut peptides and enteric nerves to brain. Physiol Behav 92(1–2):256–262

    PubMed  Google Scholar 

  • Nettle D (2006) The evolution of personality variation in humans and other animals. Am Psychol 61(6):622–631

    PubMed  Google Scholar 

  • Nyberg C (2012) Navigating transitions in HPA function from pregnancy through lactation: implications for maternal health and infant brain development. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Oftedal OT, Iverson SJ (1995) Comparative analysis of nonhuman milks: phylogenetic variation in the gross composition of milks. In: Jensen RG (ed) Handbook of milk composition. Academic, San Diego, pp 749–788

    Google Scholar 

  • Oftedal OT, Alt GL, Widdowson EM, Jakubasz MR (1993) Nutrition and growth of suckling black bears (Ursus americanus) during their mothers’ winter fast. Br J Nutr 70(1):59–79

    PubMed  CAS  Google Scholar 

  • Pácha J (2000) Development of intestinal transport function in mammals. Physiol Rev 80(4): 1633–1667

    PubMed  Google Scholar 

  • Pácha J, Miksík I (1996) 11 beta-Hydroxysteroid dehydrogenase in developing rat intestine. J Endocrinol 148(3):561–566

    PubMed  Google Scholar 

  • Parent CI, Meaney MJ (2008) The influence of natural variations in maternal care on play fighting in the rat. Dev Psychobiol 50(8):767–776

    PubMed  Google Scholar 

  • Pollard KA, Blumstein DT (2011) Social group size predicts the evolution of individuality. Curr Biol 21(5):413–417

    PubMed  CAS  Google Scholar 

  • Proulx K, Clavel S, Nault G, Richard D, Walker CD (2001) High neonatal leptin exposure enhances brain GR expression and feedback efficacy on the adrenocortical axis of developing rats. Endocrinology 142(11):4607–4616

    PubMed  CAS  Google Scholar 

  • Quinn JL, Cole EF, Bates J, Payne RW, Cresswell W (2011) Personality predicts individual responsiveness to the risks of starvation and predation. Proc Biol Sci. Epub ahead of print: doi:10.1098/rspb.2011.2227

    Google Scholar 

  • Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318

    PubMed  Google Scholar 

  • Revell DK, Williams IH, Mullan BP, Ranford JL, Smits RJ (1998) Body composition at farrowing and nutrition during lactation affect the performance of primiparous sows: II. Milk composition, milk yield, and pig growth. J Anim Sci 76(7):1738–1743

    PubMed  CAS  Google Scholar 

  • Rhee SH, Pothoulakis C, Mayer EA (2009) Principles and clinical implications of the brain-gut-enteric microbiota axis. Nat Rev Gastroenterol Hepatol 6(5):306–314

    PubMed  CAS  Google Scholar 

  • Riek A (2008) Relationship between milk energy intake and growth rate in suckling mammalian young at peak lactation: an updated meta-analysis. J Zool 274:160–170

    Google Scholar 

  • Roberts SB, Cole TJ, Coward WA (1985) Lactational performance in relation to energy intake in the baboon. Am J Clin Nutr 41:1270–1276

    PubMed  CAS  Google Scholar 

  • Rogowitz GL, McClure PA (1995) Energy export and offspring growth during lactation in cotton rats (Sigmodon hispidus). Functional Ecology 9(2):143–150

    Google Scholar 

  • 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. Dev Psychobiol 39:40–45

    PubMed  CAS  Google Scholar 

  • Rutherford JN (2012) The primate placenta as an agent of developmental and health trajectories across the lifecourse. In: Clancy KBH, Hinde K, Rutherford JN (eds) Building babies: primate development in proximate and ultimate perspectives. Springer, New York

    Google Scholar 

  • Sachser N, Hennessy MB, Kaiser S (2011) Adaptive modulation of behavioral profiles by social stress during early phase of life and adolescence. Neurosci Biobehav Rev 35:1518–1533

    PubMed  Google Scholar 

  • Sadlier RMFS (1980) Energy and protein intake in relation to growth of suckling black-tailed deer fawns. Can J Zool 58:1347–1354

    Google Scholar 

  • Sapolsky RM (1999) Hormonal correlates of personality and social context: from non-human to human primates. In: Painter-Brick C, Worthman CM (eds) Hormones, health, and behavior: a socio-ecological and lifespan perspective. Cambridge University Press, Cambridge, pp 18–46

    Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89

    PubMed  CAS  Google Scholar 

  • Savino F, Liguori SA, Fissore MF, Oggero R (2009) Breast milk hormones and their protective effect on obesity. Int J Pediatr Endocrinol. Epub 327505. doi:10.1155/2009/327505.

    Google Scholar 

  • Schuett W, Tregenza T, Dall SR (2010) Sexual selection and animal personality. Biol Rev Camb Philos Soc 85(2):217–246

    PubMed  Google Scholar 

  • Seckl JR (2004) 11beta-hydroxysteroid dehydrogenases: changing glucocorticoid action. Curr Opin Pharmacol 4(6):597–602

    PubMed  CAS  Google Scholar 

  • Sellen DW (2007) Evolution of infant and young child feeding: implications for contemporary public health. Ann Rev Nutr 27:123–148

    CAS  Google Scholar 

  • Seyfarth RM, Cheney DL (1980) The ontogeny of vervet monkey alarm-calling: a preliminary report. Z Tierpsychol 54:37–56

    Google Scholar 

  • Seyfarth RM, Cheney DL (1986) Vocal development in vervet monkeys. Animal Behaviour 34: 1640–1658

    Google Scholar 

  • Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210(4471):801–803

    PubMed  CAS  Google Scholar 

  • Sih A, Bell AM, Johnson JC, Ziemba RE (2004) Behavioral syndromes: an integrative overview. Q Rev Biol 79:241–277

    PubMed  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302(5648):1231–1234

    PubMed  CAS  Google Scholar 

  • Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc Biol Sci 276(1670):3099–3104

    PubMed  Google Scholar 

  • Siviy SM, Panksepp J (1985) Energy balance and play in juvenile rats. Physiol Behav 35:435–441

    Google Scholar 

  • Smith BR, Blumstein DT (2008) Fitness consequences of personality: a meta-analysis. Behav Ecol 19:448–455

    Google Scholar 

  • Stamps J, Groothuis TG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev Camb Philos Soc 85:301–325

    PubMed  Google Scholar 

  • Stone AI (2008) Seasonal effects on play behavior in immature Saimiri sciureus in Eastern Amazonia. International J Primatol 29:195–205

    Google Scholar 

  • Sullivan EC, Hinde K, Mendoza SP, Capitanio JP (2011) Cortisol concentrations in the milk of rhesus monkey mothers are associated with confident temperament in sons, but not daughters. Dev Psychobiol 53(1):96–104

    PubMed  CAS  Google Scholar 

  • Szyf M, Weaver I, Meaney M (2007) Maternal care, the epigenome and phenotypic differences in behavior. Reprod Toxicol 24(1):9–19

    PubMed  CAS  Google Scholar 

  • Tardif SD, Power M, 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. Behav Ecol Sociobiol 51:17–25

    Google Scholar 

  • Tibbetts EA, Dale J (2007) Individual recognition: it is good to be different. Trends Ecol Evol 22(10):529–537

    PubMed  Google Scholar 

  • Tomé D, Schwarz J, Darcel N, Fromentin G (2009) Protein, amino acids, vagus nerve signaling, and the brain. Am J Clin Nutr 90(3):838S–843S

    PubMed  Google Scholar 

  • Tomlinson JW, Walker EA, Bujalska IJ, Draper N, Lavery GG, Cooper MS, Hewison M, Stewart PM (2004) 11beta-hydroxysteroid dehydrogenase type 1: a tissue-specific regulator of glucocorticoid response. Endocr Rev 25(5):831–866

    PubMed  CAS  Google Scholar 

  • Trillmich F, Hudson R (2011) The emergence of personality in animals: the need for a developmental approach. Dev Psychobiol 53(6):505–509

    PubMed  Google Scholar 

  • Trott JF, Simpson KJ, Moyle RL, Hearn CM, Shaw G, Nicholas KR, Renfree MB (2003) Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 68(3):929–936

    PubMed  CAS  Google Scholar 

  • Trottier G, Koski KG, Brun T, Toufexis DJ, Richard D, Walker CD (1998) Increased fat intake during lactation modifies hypothalamic-pituitary-adrenal responsiveness in developing rat pups: a possible role for leptin. Endocrinology 139(9):3704–3711

    PubMed  CAS  Google Scholar 

  • Uher J (2011) Individual behavioral phenotypes: an integrative meta-theoretical framework. Why “behavioral syndromes” are not analogs of “personality. Dev Psychobiol 53(6):521–548

    PubMed  Google Scholar 

  • van Oers K, Mueller JC (2010) Evolutionary genomics of animal personality. Philos Trans R Soc Lond B Biol Sci 365(1560):3991–4000

    PubMed  Google Scholar 

  • van Schaik CP, Kappeler PM (2006) Cooperation in primates and humans: closing the gap. In: CP van Schaik, Kappeler (eds) Cooperation in primates and humans: mechanisms and evolution. Springer, pp 3–23

    Google Scholar 

  • Walker CD (2005) Nutritional aspects modulating brain development and the responses to stress in early neonatal life. Prog Neuropsychopharmacol Biol Psychiatry 29(8):1249–1263

    PubMed  CAS  Google Scholar 

  • Weinstein TAR, Capitanio JP, Gosling SD (2008) Personality in animals. In: John OP, Robinns RW, Pervin LA (eds) Handbook of personality: theory and research, 3rd edn. Guilford Press, New York, pp 328–348

    Google Scholar 

  • Wells JCK (2006) The role of cultural factors in human breastfeeding: adaptive behaviour or ­biopower? J Hum Ecol 14:39–47

    Google Scholar 

  • West-Eberhard M-J (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc Biol Sci 271(1541):819–826

    PubMed  Google Scholar 

  • Wilson LL, Gillooly JE, Rugh MC, Thompson CE, Purdy HR (1969) Effects of energy intake, cow body size and calf sex on composition and yield of milk by Angus-Holstein cows and preweaning growth rate of progeny. J Anim Sci 28(6):789–795

    PubMed  CAS  Google Scholar 

  • Wisse BE, Schwartz MW (2003) The skinny on neurotrophins. Nat Neurosci 6(7):655–656

    PubMed  CAS  Google Scholar 

  • Wolf M, Weissing FJ (2010) An explanatory framework for adaptive personality differences. Philos Trans R Soc Lond B Biol Sci 365(1560):3959–3968

    PubMed  Google Scholar 

  • Wolf M, Sander van Doorn G, Leimar O, Weissing FJ (2007) Life-history tradeoffs favor the evolution of animal personalities. Nature 447:581–584

    PubMed  CAS  Google Scholar 

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Acknowledgments

I thank Alicia Beakey, Katharine Campi, John Capitanio, Kate Clancy, Nicole Maninger, Stephanie Meredith, Todd Mitchell, Justin Moscarello, Julienne Rutherford, Joan Silk, Tamara Weinstein, and two anonymous reviewers for valuable comments on earlier versions of this chapter. I particularly thank Danielle Lemay for generously allowing me to use her “magic potion” metaphor at the outset of this chapter and Grant Lampard for his photo of an infant rhesus macaque.

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Hinde, K. (2013). Lactational Programming of Infant Behavioral Phenotype. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_9

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