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Published in: BMC Medicine 1/2013

Open Access 01-12-2013 | Research article

Effects of breastfeeding on body composition and maturational tempo in the rat

Authors: Yonatan Crispel, Oren Katz, Dafna Ben-Yosef, Ze'ev Hochberg

Published in: BMC Medicine | Issue 1/2013

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Abstract

Background

Features of life history are subject to environmental regulation in the service of reproductive fitness goals. We have previously shown that the infant-to-childhood transition reflects the adaptive adjustment of an individual's size to the prevailing and anticipated environment.

Methods

To evaluate effects of weaning age on life-history traits in rats, we repeatedly measured length and body mass index (BMI), as well as physiological development and sexual maturation in pups weaned early (d16), normally (d21) or late (d26). Males were bred to females of the same weaning age group for four generations.

Results

Here, we show that the age at weaning from lactation regulates a rat's life history, growth, body composition and maturational tempo. We show that early-weaned rats developed faster than normal- or late-weaned rats; they are leaner and longer than late-weaned ones who are heavier and shorter. Early-weaned progeny develop more rapidly (that is, fur budding, pinnae detachment, eye opening); females show earlier vaginal opening and estrous and males show earlier onset of testicular growth. In generations 3 and 4, early-weaned rats bear larger litter sizes and heavier newborn pups. The entire traits complex is transmitted to subsequent generations from the paternal side.

Conclusions

The findings presented here lend support to the proposition that the duration of infancy, as indexed by weaning age, predicts and perhaps programs growth, body composition, and the tempo of physiological development and maturation, as well as litter size and parity and, thereby, reproductive strategy.
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Literature
1.
go back to reference 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: Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011, 32: 159-224. 10.1210/er.2009-0039.CrossRefPubMed 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: Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011, 32: 159-224. 10.1210/er.2009-0039.CrossRefPubMed
3.
go back to reference Smith B: Life history and the evolution of human maturation. Evol Anthropol. 1992, 1: 134-142.CrossRef Smith B: Life history and the evolution of human maturation. Evol Anthropol. 1992, 1: 134-142.CrossRef
4.
go back to reference Hochberg Z: Evo-devo of child growth II: human life history and transition between its phases. Eur J Endocrinol. 2009, 160: 135-141.CrossRefPubMed Hochberg Z: Evo-devo of child growth II: human life history and transition between its phases. Eur J Endocrinol. 2009, 160: 135-141.CrossRefPubMed
5.
go back to reference Hochberg Z, Albertsson-Wikland K: Evo-devo of infantile and childhood growth. Pediatr Res. 2008, 64: 2-7. 10.1203/PDR.0b013e318177590f.CrossRefPubMed Hochberg Z, Albertsson-Wikland K: Evo-devo of infantile and childhood growth. Pediatr Res. 2008, 64: 2-7. 10.1203/PDR.0b013e318177590f.CrossRefPubMed
6.
go back to reference Hochberg Z: Evo Devo of Child Growth: Treatize on Child Growth and Human Evolution. 2012, New York, NY: Wiley Hochberg Z: Evo Devo of Child Growth: Treatize on Child Growth and Human Evolution. 2012, New York, NY: Wiley
7.
go back to reference Cook CJ: Patterns of weaning and adult response to stress. Physiol Behav. 1999, 67: 803-808. 10.1016/S0031-9384(99)00107-9.CrossRefPubMed Cook CJ: Patterns of weaning and adult response to stress. Physiol Behav. 1999, 67: 803-808. 10.1016/S0031-9384(99)00107-9.CrossRefPubMed
8.
go back to reference Caldji C, Diorio J, Meaney MJ: Variations in maternal care alter GABA(A) receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology. 2003, 28: 1950-1959. 10.1038/sj.npp.1300237.CrossRefPubMed Caldji C, Diorio J, Meaney MJ: Variations in maternal care alter GABA(A) receptor subunit expression in brain regions associated with fear. Neuropsychopharmacology. 2003, 28: 1950-1959. 10.1038/sj.npp.1300237.CrossRefPubMed
9.
go back to reference McGowan PO, Suderman M, Sasaki A, Huang TC, Hallett M, Meaney MJ, Szyf M: Broad epigenetic signature of maternal care in the brain of adult rats. PLoS One. 2011, 6: e14739-10.1371/journal.pone.0014739.CrossRefPubMedPubMedCentral McGowan PO, Suderman M, Sasaki A, Huang TC, Hallett M, Meaney MJ, Szyf M: Broad epigenetic signature of maternal care in the brain of adult rats. PLoS One. 2011, 6: e14739-10.1371/journal.pone.0014739.CrossRefPubMedPubMedCentral
10.
go back to reference Denenberg VH, Grota LJ, Zarrow MX: Maternal behaviour in the rat: analysis of cross-fostering. J Reprod Fertil. 1963, 5: 133-141. 10.1530/jrf.0.0050133.CrossRefPubMed Denenberg VH, Grota LJ, Zarrow MX: Maternal behaviour in the rat: analysis of cross-fostering. J Reprod Fertil. 1963, 5: 133-141. 10.1530/jrf.0.0050133.CrossRefPubMed
11.
go back to reference Heyser CJ: UNIT 8.18 Assessment of developmental milestones in rodents. Current Protocols in Neuroscience. 2003, Hoboken, NJ: Wiley-Blackwell, 8.18.11-18.18.15. Heyser CJ: UNIT 8.18 Assessment of developmental milestones in rodents. Current Protocols in Neuroscience. 2003, Hoboken, NJ: Wiley-Blackwell, 8.18.11-18.18.15.
12.
go back to reference Prader A: Testicular size: assessment and clinical importance. Triangle. 1966, 7: 240-243.PubMed Prader A: Testicular size: assessment and clinical importance. Triangle. 1966, 7: 240-243.PubMed
13.
go back to reference Halldorsdottir S, Carmody J, Boozer CN, Leduc CA, Leibel RL: Reproducibility and accuracy of body composition assessments in mice by dual energy x-ray absorptiometry and time domain nuclear magnetic resonance. Int J Body Compos Res. 2009, 7: 147-154.PubMedPubMedCentral Halldorsdottir S, Carmody J, Boozer CN, Leduc CA, Leibel RL: Reproducibility and accuracy of body composition assessments in mice by dual energy x-ray absorptiometry and time domain nuclear magnetic resonance. Int J Body Compos Res. 2009, 7: 147-154.PubMedPubMedCentral
14.
go back to reference Bruning JC, Winnay J, Bonner-Weir S, Taylor SI, Accili D, Kahn CR: Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell. 1997, 88: 561-572. 10.1016/S0092-8674(00)81896-6.CrossRefPubMed Bruning JC, Winnay J, Bonner-Weir S, Taylor SI, Accili D, Kahn CR: Development of a novel polygenic model of NIDDM in mice heterozygous for IR and IRS-1 null alleles. Cell. 1997, 88: 561-572. 10.1016/S0092-8674(00)81896-6.CrossRefPubMed
15.
go back to reference Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ: The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005, 29: 843-865. 10.1016/j.neubiorev.2005.03.022.CrossRefPubMed Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ: The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005, 29: 843-865. 10.1016/j.neubiorev.2005.03.022.CrossRefPubMed
16.
go back to reference Belsky J, Fearon RM: Early attachment security, subsequent maternal sensitivity, and later child development: does continuity in development depend upon continuity of caregiving?. Attach Hum Dev. 2002, 43: 361-387.CrossRef Belsky J, Fearon RM: Early attachment security, subsequent maternal sensitivity, and later child development: does continuity in development depend upon continuity of caregiving?. Attach Hum Dev. 2002, 43: 361-387.CrossRef
17.
go back to reference Del Giudice M: Sex, attachment, and the development of reproductive strategies. Behav Brain Sci. 2009, 32: 1-21. 10.1017/S0140525X09000016. discussion 21-67CrossRefPubMed Del Giudice M: Sex, attachment, and the development of reproductive strategies. Behav Brain Sci. 2009, 32: 1-21. 10.1017/S0140525X09000016. discussion 21-67CrossRefPubMed
18.
go back to reference Zimmerberg B, Weston HE: Postnatal stress of early weaning exacerbates behavioral outcome in prenatal alcohol-exposed juvenile rats. Pharmacol Biochem Behav. 2002, 73: 45-52. 10.1016/S0091-3057(02)00797-9.CrossRefPubMed Zimmerberg B, Weston HE: Postnatal stress of early weaning exacerbates behavioral outcome in prenatal alcohol-exposed juvenile rats. Pharmacol Biochem Behav. 2002, 73: 45-52. 10.1016/S0091-3057(02)00797-9.CrossRefPubMed
19.
go back to reference Costa E, Amaral Filha WS, Costa AHA, Carvalho FF, Santos AK, Silva AF: Influence of the lactation length in the subsequent litter size of sows. Anim Reprod. 2004, 1: 111-114. Costa E, Amaral Filha WS, Costa AHA, Carvalho FF, Santos AK, Silva AF: Influence of the lactation length in the subsequent litter size of sows. Anim Reprod. 2004, 1: 111-114.
20.
go back to reference Haig D: Colloquium papers: Transfers and transitions: parent-offspring conflict, genomic imprinting, and the evolution of human life history. Proc Natl Acad Sci USA. 2010, 107 (Suppl 1): 1731-1735.CrossRefPubMedPubMedCentral Haig D: Colloquium papers: Transfers and transitions: parent-offspring conflict, genomic imprinting, and the evolution of human life history. Proc Natl Acad Sci USA. 2010, 107 (Suppl 1): 1731-1735.CrossRefPubMedPubMedCentral
21.
go back to reference Hager R, Johnstone RA: The genetic basis of family conflict resolution in mice. Nature. 2003, 421: 533-535. 10.1038/nature01239.CrossRefPubMed Hager R, Johnstone RA: The genetic basis of family conflict resolution in mice. Nature. 2003, 421: 533-535. 10.1038/nature01239.CrossRefPubMed
22.
go back to reference Neel JV: Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?. Am J Hum Genet. 1962, 14: 353-362.PubMedPubMedCentral Neel JV: Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"?. Am J Hum Genet. 1962, 14: 353-362.PubMedPubMedCentral
23.
go back to reference Wells JC: The thrifty phenotype hypothesis: thrifty offspring or thrifty mother?. J Theor Biol. 2003, 221: 143-161. 10.1006/jtbi.2003.3183.CrossRefPubMed Wells JC: The thrifty phenotype hypothesis: thrifty offspring or thrifty mother?. J Theor Biol. 2003, 221: 143-161. 10.1006/jtbi.2003.3183.CrossRefPubMed
24.
go back to reference Belsky J, Steinberg L, Draper P: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization. Child Dev. 1991, 62: 647-670. 10.2307/1131166.CrossRefPubMed Belsky J, Steinberg L, Draper P: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization. Child Dev. 1991, 62: 647-670. 10.2307/1131166.CrossRefPubMed
Metadata
Title
Effects of breastfeeding on body composition and maturational tempo in the rat
Authors
Yonatan Crispel
Oren Katz
Dafna Ben-Yosef
Ze'ev Hochberg
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-11-114

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