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Evolution of lactation: nutrition v. protection with special reference to five mammalian species

  • Holly L. McClellan (a1), Susan J. Miller (a2) and Peter E. Hartmann (a1)
Abstract

The evolutionary origin of the mammary gland has been difficult to establish because little knowledge can be gained on the origin of soft tissue organs from fossil evidence. One approach to resolve the origin of lactation has compared the anatomy of existing primitive mammals to skin glands, whilst another has examined the metabolic and molecular synergy between mammary gland development and the innate immune system. We have reviewed the physiology of lactation in five mammalian species with special reference to these theories. In all species, milk fulfils dual functions of providing protection and nutrition to the young and, furthermore, within species the quality and quantity of milk are highly conserved despite maternal malnutrition or illness. There are vast differences in birth weight, milk production, feeding frequency, macronutrient concentration, growth rate and length of lactation between rabbits, quokkas (Setonix brachyurus), pigs, cattle and humans. The components that protect the neonate against infection do so without causing inflammation. Many protective components are not unique to the mammary gland and are shared with the innate immune system. In contrast, many of the macronutrients in milk are unique to the mammary gland, have evolved from components of the innate immune system, and have either retained or developed multiple functions including the provision of nourishment and protection of the hatchling/neonate. Thus, there is a strong argument to suggest that the mammary gland evolved from the inflammatory response; however, the extensive protection that has developed in milk to actively avoid triggering inflammation seems to be a contradiction.

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Corresponding author
*Corresponding author: H. L. McClellan, fax +61 8 6488 1148, email hlm@student.uwa.edu.au
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1 L Schiebinger (1993) Why mammals are called mammals: gender politics in eighteenth-century natural history. Am Hist Rev 98, 382411.

5 C Vorbach , MR Capecchi & JM Penninger (2006) Evolution of the mammary gland from the innate immune system? Bioessays 28, 606616.

6 D Brawand , W Wahli & H Kaessmann (2008) Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biol 6, e63.

7 C Vorbach , A Scriven & MR Capecchi (2002) The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes Dev 16, 32233235.

8 C Vorbach , R Harrison & MR Capecchi (2003) Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends Immunol 24, 512517.

9 Y Cao , G Bonizzi , TN Seagroves , . (2001) IKKα provides an essential link between RANK signaling and cyclin D1 expression during mammary gland development. Cell 107, 763775.

10 C Brisken (2002) Hormonal control of alveolar development and its implications for breast carcinogenesis. J Mammary Gland Biol Neoplasia 7, 3948.

11 K Nishimori , LJ Young , Q Guo , . (1996) Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A 93, 1169911704.

12 S Friedrichsen , CV Harper , S Semprini , . (2006) Tumor necrosis factor-α activates the human prolactin gene promoter via nuclear factor-κB signaling. Endocrinology 147, 773781.

13 V Terzidou , Y Lee , T Lindstrom , . (2006) Regulation of the human oxytocin receptor by nuclear factor-κB and CCAAT/enhancer-binding protein-β. J Clin Endocrinol Metab 91, 23172326.

14 DP Ramji & P Foka (2002) CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J 365, 561575.

15 TN Seagroves , S Krnacik , B Raught , . (1998) C/EBPβ, but not C/EBPα, is essential for ductal morphogenesis, lobuloalveolar proliferation, and functional differentiation in the mouse mammary gland. Genes Dev 12, 19171928.

16 CW Chow , MP Clark , JE Rinaldo , . (1995) Multiple initiators and C/EBP binding sites are involved in transcription from the TATA-less rat XDH/XO basal promoter. Nucleic Acids Res 23, 31323140.

17 R Nanbu-Wakao , Y Fujitani , Y Masuho , . (2000) Prolactin enhances CCAAT enhancer-binding protein-β (C/EBPβ) and peroxisome proliferator-activated receptor γ (PPARγ) messenger RNA expression and stimulates adipogenic conversion of NIH-3T3 cells. Mol Endocrinol 14, 307316.

18 M Kawai , N Namba , S Mushiake , . (2007) Growth hormone stimulates adipogenesis of 3T3-L1 cells through activation of the Stat5A/5B-PPARγ pathway. J Mol Endocrinol 38, 1934.

19 Y Wan , A Saghatelian , LW Chong , . (2007) Maternal PPARγ protects nursing neonates by suppressing the production of inflammatory milk. Genes Dev 21, 18951908.

20 AJ Vidal-Puig , RV Considine , M Jimenez-Linan , . (1997) Peroxisome proliferator-activated receptor gene expression in human tissues. Effects of obesity, weight loss, and regulation by insulin and glucocorticoids. J Clin Invest 99, 24162422.

21 DP Hewitt , PJ Mark & BJ Waddell (2006) Placental expression of peroxisome proliferator-activated receptors in rat pregnancy and the effect of increased glucocorticoid exposure. Biol Reprod 74, 2328.

22 C Darwin (1902) On the Origin of Species by Means of Natural Selection or the Preservation of Favoured Races in the Struggle for Life. London: Grant Richards.

23 OT Oftedal & SA Iverson (1995) Comparative analysis of nonhuman milks. A. Phylogenetic variation in the gross composition of milks. In Handbook of Milk Composition, pp. 749789 [ RG Jensen , editor]. San Diego, CA: Academic Press.

25 CH Tyndale-Biscoe & PA Janssens (1988) Introduction. In The Developing Marsupial: Models for Biomedical Research, pp. 17 [ CH Tyndale-Biscoe and PA Janssens , editors]. Berlin: Springer-Verlag.

30 J Shield (1968) Reproduction of the quokka, Setonix brachyurus, in captivity. J Zool (Lond) 155, 427444.

31 JF Trott , KJ Simpson , RLC Moyle , . (2003) Maternal regulation of milk composition, milk production, and pouch young development during lactation in the tammar wallaby (Macropus eugenii). Biol Reprod 68, 929936.

32 AT Cowie (1969) Variations in the yield and composition of the milk during lactation in the rabbit and the galactopoietic effect of prolactin. J Endocrinol 44, 437450.

34 CH Tyndale-Biscoe (2001) Australasian marsupials – to cherish and to hold. Reprod Fertil Dev 13, 477485.

37 A Gooneratne , PE Hartmann , I McCauley , . (1979) Control of parturition in the sow using progesterone and prostaglandin. Aust J Biol Sci 32, 587595.

41 DB Coates , L Mannetje & GW Seifert (1987) Reproductive performance and calf growth to weaning of Hereford and Belmont Red cattle in subtropical, subcoastal Queensland. Aust J Exp Agric 27, 110.

42 AM Grondahl , EM Skancke , CM Mejdell , . (2007) Growth rate, health and welfare in a dairy herd with natural suckling until 6–8 weeks of age: a case report. Acta Vet Scand 49, 16.

45 SJ Fomon & SE Nelson (2002) Body composition of the male and female reference infants. Annu Rev Nutr 22, 117.

48 IG Wickes (1953) A history of infant feeding. I. Primitive peoples; ancient works; Renaissance writers. Arch Dis Child 28, 151158.

50 TJ Case (1978) On the evolution and adaptive significance of postnatal growth rates in the terrestrial vertebrates. Q Rev Biol 53, 243282.

51 M Konner & C Worthman (1980) Nursing frequency, gonadal function, and birth spacing among !Kung hunter-gatherers. Science 207, 788791.

53 M Rendle-Short & J Rendle-Short (1966) The Father of Child Care. Life of William Cadogan (1711–1797). Bristol: John Wright and Sons Ltd.

56 SE Daly , RA Owens & PE Hartmann (1993) The short-term synthesis and infant-regulated removal of milk in lactating women. Exp Physiol 78, 209220.

59 JG Wickes (1953) A history of infant feeding. IV. Nineteenth century continued. Arch Dis Child 28, 416422.

61 JC Kent , LR Mitoulas , MD Cregan , . (2006) Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pediatrics 117, e387e395.

62 JA Sharp , KN Cane , C Lefevre , . (2006) Fur seal adaptations to lactation: insights into mammary gland function. Curr Top Dev Biol 72, 275308.

66 MX Zarrow , VH Denenberg & CO Anderson (1965) Rabbit: frequency of suckling in the pup. Science 150, 18351836.

70 A Argiolas & GL Gessa (1991) Central functions of oxytocin. Neurosci Biobehav Rev 15, 217231.

71 JS Tindal & GS Knaggs (1969) An ascending pathway for release of prolactin in the brain of the rabbit. J Endocrinol 45, 111120.

72 AM Blanks , A Shmygol & S Thornton (2007) Regulation of oxytocin receptors and oxytocin receptor signaling. Semin Reprod Med 25, 5259.

73 KK Smith (2001) Early development of the neural plate, neural crest and facial region of marsupials. J Anat 199, 121131.

77 GM Ardran , FH Kemp & J Lind (1958) A cineradiographic study of bottle feeding. Br J Radiol 31, 1122.

79 DT Geddes , JC Kent , LR Mitoulas , . (2008) Tongue movement and intra-oral vacuum in breastfeeding infants. Early Hum Dev 84, 471477.

80 AJ Thexton , AW Crompton , T Owerkowicz , . (2004) Correlation between intraoral pressures and tongue movements in the suckling pig. Arch Oral Biol 49, 567575.

81 MD Rasmussen & M Mayntz (1998) Pressure in the teat cistern and the mouth of the calf during suckling. J Dairy Res 65, 685692.

82 DT Ramsay , JC Kent , RA Hartmann , . (2005) Anatomy of the lactating human breast redefined with ultrasound imaging. J Anat 206, 525534.

84 JR Cannon , HR Bakker , SD Bradshaw , . (1976) Gravity as the sole navigational aid to the newborn quokka. Nature 259, 42.

85 AM Widstrom , AB Ransjo-Arvidson , K Christensson , . (1987) Gastric suction in healthy newborn infants. Effects on circulation and developing feeding behaviour. Acta Paediatr Scand 76, 566572.

87 JM Diamond (1987) Evolutionary adaptations. Aristotle's theory of mammalian teat number is confirmed. Nature 325, 200.

89 CG Prosser , L Saint & PE Hartmann (1984) Mammary gland function during gradual weaning and early gestation in women. Aust J Exp Biol Med Sci 62, 215228.

90 KG Dewey & B Lonnerdal (1986) Infant self-regulation of breast milk intake. Acta Paediatr Scand 75, 893898.

91 R Sosa , M Klaus & JJ Urrutia (1976) Feed the nursing mother, thereby the infant. J Pediatr 88, 668670.

93 B Lonnerdal (2000) Breast milk: a truly functional food. Nutrition 16, 509511.

94 PG Arthur , JC Kent & PE Hartmann (1991) Metabolites of lactose synthesis in milk from women during established lactation. J Pediatr Gastroenterol Nutr 13, 260266.

95 P McVeagh & JB Miller (1997) Human milk oligosaccharides: only the breast. J Paediatr Child Health 33, 281286.

97 WW Pang & PE Hartmann (2007) Initiation of human lactation: secretory differentiation and secretory activation. J Mammary Gland Biol Neoplasia 12, 211221.

98 CH Tyndale-Biscoe & PA Janssens (1988) The Developing Marsupial: Models for Biomedical Research. Berlin: Springer-Verlag.

99 RG Jensen (1995) Handbook of Milk Composition. San Diego, CA: Academic Press.

101 M Neville , J Allen & C Watters (1983) The mechanisms of milk secretion. In Lactation: Physiology, Nutrition and Breastfeeding, pp. 49102 [ M Neville and M Neifert , editors]. New York: Plenum Press.

103 PC Shekar , S Goel , SD Rani , . (2006) κ-Casein-deficient mice fail to lactate. Proc Natl Acad Sci U S A 103, 80008005.

105 JM Gooden , MR Brandon , PE Hartmann , . (1971) Factors affecting lipid output and flow of thoracic duct lymph in newborn calves. Aust J Biol Sci 24, 13091318.

106 SM Jordan & EH Morgan (1968) The changes in the serum and milk whey proteins during lactation and suckling in the quokka (Setonix brachyurus). Comp Biochem Physiol 25, 271283.

107 KJ Simpson , S Ranganathan , JA Fisher , . (2000) The gene for a novel member of the whey acidic protein family encodes three four-disulfide core domains and is asynchronously expressed during lactation. J Biol Chem 275, 2307423081.

108 CP Piotte , CJ Marshall , MJ Hubbard , . (1997) Lysozyme and α-lactalbumin from the milk of a marsupial, the common brush-tailed possum (Trichosurus vulpecula). Biochim Biophys Acta 1336, 235242.

109 V Hayssen & D Blackburn (1985) α-Lactalbumin and the origins of lactation. Evolution 39, 11471149.

110 G Kontopidis , C Holt & L Sawyer (2004) Invited review: β-lactoglobulin: binding properties, structure, and function. J Dairy Sci 87, 785796.

111 C Collet , R Joseph & K Nicholas (1991) A marsupial β-lactoglobulin gene: characterization and prolactin-dependent expression. J Mol Endocrinol 6, 916.

112 B Hernández-Ledesma , I Recio & L Amigo (2007) β-Lactoglobulin as source of bioactive peptides. Amino Acids 35, 257265.

113 JC Martin , P Bougnoux , JM Antoine , . (1993) Triacylglycerol structure of human colostrum and mature milk. Lipids 28, 637643.

114 WC Breckenridge , L Marai & A Kuksis (1969) Triglyceride structure of human milk fat. Can J Biochem 47, 761769.

116 SL Ogg , AK Weldon , L Dobbie , . (2004) Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. Proc Natl Acad Sci U S A 101, 1008410089.

117 M Cavaletto , MG Giuffrida , C Giunta , . (1999) Multiple forms of lactadherin (breast antigen BA46) and butyrophilin are secreted into human milk as major components of milk fat globule membrane. J Dairy Res 66, 295301.

118 MC Michalski , V Briard , F Michel , . (2005) Size distribution of fat globules in human colostrum, breast milk, and infant formula. J Dairy Sci 88, 19271940.

120 SJ Iverson & OT Oftedal (1995) Comparative analysis of nonhuman milks. B. Phylogenetic and ecological variation in the fatty acid composition of milks. In Handbook of Milk Composition, pp. 789827 [ RG Jensen , editor]. San Diego, CA: Academic Press.

122 RJ Moir , G Sharman , M Somers , . (1954) Ruminant-like digestion in a marsupial. Nature 173, 269270.

123 L Hartman , FB Shorland & IRC McDonald (1955) The trans-unsaturated acid contents of fats of ruminants and non-ruminants. Biochem J 61, 603607.

125 AT Cowie , IA Forsyth & IC Hart (1980) Monographs on Endocrinology, Hormonal Control of Lactation, vol. 15. Berlin: Springer-Verlag.

128 M Yadav , M Eadie & NF Stanley (1972) The thymus glands of a marsupial, Setonix brachyurus (quokka) and their role in immune responses. VI. Maternal transfer of immunoglobulins. Aust J Exp Biol Med Sci 50, 347356.

129 M Yadav & M Eadie (1973) Passage of maternal immunoglobulins to the pouch young of a marsupial, Setonix brachyurus. Aust J Zool 21, 171181.

131 AS Goldman , S Chheda & R Garofalo (1998) Evolution of immunologic functions of the mammary gland and the postnatal development of immunity. Pediatr Res 43, 155162.

132 DS Newburg & SH Neubauer (1995) Carbohydrates in milks: analysis, quantities, and significance. In Handbook of Milk Composition, pp. 273349 [ RG Jensen , editor]. San Diego, CA: Academic Press.

133 AD Leman (1992) Optimizing farrowing rate and litter size and minimizing nonproductive sow days. Vet Clin North Am Food Anim Pract 8, 609621.

136 DI Campbell , JE Bunn , LT Weaver , . (2006) Human milk vacuolating cytotoxin A immunoglobulin A antibodies modify Helicobacter pylori infection in Gambian children. Clin Infect Dis 43, 10401042.

137 LM Freed , SE Berkow , P Hamosh , . (1989) Lipases in human milk: effect of gestational age and length of lactation on enzyme activity. J Am Coll Nutr 8, 143150.

142 M Yadav , NF Stanley & H Waring (1972) The microbial flora of the gut of the pouch-young and the pouch of a marsupial, Setonix brachyurus. J Gen Microbiol 70, 437442.

144 DW Dellow & ID Hume (1982) Studies on the nutrition of macropodine marsupials IV. Digestion in the stomach and the intestine of Macropus giganteus, Thylogale thetis and Macropus eugenii. Aust J Zool 30, 767777.

146 SJ Bell , GT Grochoski & AJ Clarke (2006) Health implications of milk containing β-casein with the A2 genetic variant. Crit Rev Food Sci Nutr 46, 93100.

149 A Pellegrini , U Thomas , N Bramaz , . (1999) Isolation and identification of three bactericidal domains in the bovine α-lactalbumin molecule. Biochim Biophys Acta 1426, 439448.

150 JJ Bullen , HJ Rogers & L Leigh (1972) Iron-binding proteins in milk and resistance to Escherichia coli infection in infants. BMJ 1, 6975.

151 WH Oddy , PG Holt , PD Sly , . (1999) Association between breast feeding and asthma in 6 year old children: findings of a prospective birth cohort study. BMJ 319, 815819.

153 CE Isaacs , H Thormar & T Pessolano (1986) Membrane-disruptive effect of human milk: inactivation of enveloped viruses. J Infect Dis 154, 966971.

154 DS Reiner , CS Wang & FD Gillin (1986) Human milk kills Giardia lamblia by generating toxic lipolytic products. J Infect Dis 154, 825832.

155 IH Mather & LJ Jack (1993) A review of the molecular and cellular biology of butyrophilin, the major protein of bovine milk fat globule membrane. J Dairy Sci 76, 38323850.

157 B Green , J Merchant & K Newgrain (1997) Lactational energetics of a marsupial carnivore, the eastern quoll (Dasyurus viverrinus). Aust J Zool 45, 295306.

161 B Lonnerdal , N Zavaleta , L Kusunoki , . (1996) Effect of postpartum maternal infection on proteins and trace elements in colostrum and early milk. Acta Paediatr 85, 537542.

165 W Insull Jr & EH Ahrens Jr (1959) The fatty acids of human milk from mothers on diets taken ad libitum. Biochem J 72, 2733.

166 SE Daly , A Di Rosso , RA Owens , . (1993) Degree of breast emptying explains changes in the fat content, but not fatty acid composition, of human milk. Exp Physiol 78, 741755.

170 CS Atwood & RL Bowen (2007) Metabolic clues regarding the enhanced performance of elite endurance athletes from orchiectomy-induced hormonal changes. Med Hypotheses 68, 735749.

171 MC Rudolph , JL McManaman , T Phang , . (2007) Metabolic regulation in the lactating mammary gland: a lipid synthesizing machine. Physiol Genomics 28, 323336.

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