Skip to main content

The evolution of milk secretion and its ancient origins

  • O. T. Oftedal (a1)

Lactation represents an important element of the life history strategies of all mammals, whether monotreme, marsupial, or eutherian. Milk originated as a glandular skin secretion in synapsids (the lineage ancestral to mammals), perhaps as early as the Pennsylvanian period, that is, approximately 310 million years ago (mya). Early synapsids laid eggs with parchment-like shells intolerant of desiccation and apparently dependent on glandular skin secretions for moisture. Mammary glands probably evolved from apocrine-like glands that combined multiple modes of secretion and developed in association with hair follicles. Comparative analyses of the evolutionary origin of milk constituents support a scenario in which these secretions evolved into a nutrient-rich milk long before mammals arose. A variety of antimicrobial and secretory constituents were co-opted into novel roles related to nutrition of the young. Secretory calcium-binding phosphoproteins may originally have had a role in calcium delivery to eggs; however, by evolving into large, complex casein micelles, they took on an important role in transport of amino acids, calcium and phosphorus. Several proteins involved in immunity, including an ancestral butyrophilin and xanthine oxidoreductase, were incorporated into a novel membrane-bound lipid droplet (the milk fat globule) that became a primary mode of energy transfer. An ancestral c-lysozyme lost its lytic functions in favor of a role as α-lactalbumin, which modifies a galactosyltransferase to recognize glucose as an acceptor, leading to the synthesis of novel milk sugars, of which free oligosaccharides may have predated free lactose. An ancestral lipocalin and an ancestral whey acidic protein four-disulphide core protein apparently lost their original transport and antimicrobial functions when they became the whey proteins β-lactoglobulin and whey acidic protein, which with α-lactalbumin provide limiting sulfur amino acids to the young. By the late Triassic period (ca 210 mya), mammaliaforms (mammalian ancestors) were endothermic (requiring fluid to replace incubatory water losses of eggs), very small in size (making large eggs impossible), and had rapid growth and limited tooth replacement (indicating delayed onset of feeding and reliance on milk). Thus, milk had already supplanted egg yolk as the primary nutrient source, and by the Jurassic period (ca 170 mya) vitellogenin genes were being lost. All primary milk constituents evolved before the appearance of mammals, and some constituents may have origins that predate the split of the synapsids from sauropsids (the lineage leading to ‘reptiles’ and birds). Thus, the modern dairy industry is built upon a very old foundation, the cornerstones of which were laid even before dinosaurs ruled the earth in the Jurassic and Cretaceous periods.

Corresponding author
Hide All
Akerstrom, B, Borregaard, N, Flower, DR, Salier, J-P 2006. Lipocalins. Landes Bioscience, Georgetown, TX.
Ali, MF, Lips, KR, Knoop, FC, Fritzsch, B, Miller, C, Conlon, JM 2002. Antimicrobial peptides and protease inhibitors in the skin secretions of the crawfish frog, Rana areolata. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics 1601, 5563.
Andrechek, ER, Mori, S, Rempel, RE, Chang, JT, Nevins, JR 2008. Patterns of cell signaling pathway activation that characterize mammary development. Development 135, 24032413.
Arnould, JPY, Boyd, IL 1995. Temporal patterns of milk production in Antarctic fur seals (Arctocephalus gazella). Journal of Zoology 237, 112.
Arnould, JPY, Boyd, IL, Socha, DG 1996. Milk consumption and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups. Canadian Journal of Zoology 74, 254266.
Beck, G, Habicht, GS 1996. Immunity and the invertebrates. Scientific American 275, 6063, 66.
Beutler, B 2004. Innate immunity: an overview. Molecular Immunology 40, 845859.
Bingle, CD, Vyakarnam, A 2008. Novel innate immune functions of the whey acidic protein family. Trends in Immunology 29, 444453.
Bingle, L, Cross, SS, High, AS, Wallace, WA, Rassl, D, Yuan, G, Hellstrom, I, Campos, MA, Bingle, CD 2006. WFDC2 (HE4): a potential role in the innate immunity of the oral cavity and respiratory tract and the development of adenocarcinomas of the lung. Respiratory Research 7, 6170.
Blackburn, DG 2006. Squamate reptiles as model organisms for the evolution of viviparity. Herpetological Monographs 20, 131146.
Brawand, D, Wahli, W, Kaessmann, H 2008. Loss of egg yolk genes in mammals and the origin of lactation and placentation. PLoS Biology 6, e63. doi:10.1371/journal.pbio.0060063.
Bresslau, E 1912. Die entwickelung des mammarapparates der monotremen, marsupialier und einiger placentallier. III. Entwickelung des mammarapparates der marsupialier, insectivoren, nagatheire, carnivoren und widerkauer. Jenaische Denkschriften 7, 647874, plates 637–646.
Bresslau, E 1920. The mammary apparatus of the mammals in light of ontogenesis and phylogenesis. Methuen, London, UK.
Brew, K 2003. α-lactalbumin. In Advanced Dairy Chemistry – I. Proteins. Part A (ed. PF Fox and P McSweeney), pp. 387419. Kluver Academic, New York, NY.
Buckley, J, Maunder, RJ, Foey, A, Pearce, J, Val, AL, Sloman, KA 2010. Biparental mucus feeding: a unique example of parental care in an Amazonian cichlid. The Journal of Experimental Biology 213, 37873795.
Burns, RA, Milner, JA 1981. Sulfur amino acid requirements of immature Beagle dogs. The Journal of Nutrition 111, 21172124.
Callewaert, L, Michiels, CW 2010. Lysozymes in the animal kingdom. Journal of Biosciences 35, 127160.
Capuco, AV, Akers, RM 2009. Minireview. The origin and evolution of lactation. Journal of Biology 8, 37. doi:10.1186/jbiol139
Chudinov, P 1968. Structure of the integuments of thermomorphs. Doklady Academy of Sciences USSR Earth Science Section 179, 226229.
Clarke, B 1997. The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biological Reviews 72, 365379.
Crisp, EA, Messer, M, Cowan, PE 1989. Intestinal lactase (β-galactosidase) and other disaccharidase activities of suckling and adult common brushtail possums, Trichosurus vulpecula (Marsupialia: Phalangeridae). Reproduction, Fertility, and Development 1, 315324.
Darwin, C 1872. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle of life. John Murray, London, UK.
Demmer, J, Ross, IK, Ginger, MR, Piotte, CK, Grigor, MR 1998. Differential expression of milk protein genes during lactation in the common brushtail possum (Trichosurus vulpecula). Journal of Molecular Endocrinology 20, 3744.
Dhouailly, D 2009. A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of Anatomy 214, 587606.
Enroth, C, Eger, BT, Okamoto, K, Nishino, T, Pai, EF 2000. Crystal structures of bovine milk xanthine dehydrogenase and xanthine oxidase: structure-based mechanism of conversion. Proceedings of the National Academy of Sciences of the United States of America 97, 1072310728.
Flower, DR 1996. The lipocalin protein family: structure and function. The Biochemical Journal 318, 114.
Foldager, J, Huber, JT, Bergen, WG 1977. Methionine and sulfur amino acid requirement in the preruminant calf. Journal of Dairy Science 60, 10951104.
Fomon, SJ, Ziegler, EE, Nelson, SE, Edwards, BB 1986. Requirement for sulfur-containing amino acids in infancy. The Journal of Nutrition 116, 14051422.
Fox, PF 2003. Milk proteins: general and historical aspects. In Advanced dairy chemistry – I. Proteins. Part A (ed. PF Fox and P McSweeney), pp. 148. Kluwer Academic, New York, NY.
Fry, BG, Scheib, H, van der Weerd, L, Young, B, McNaughtan, J, Ramjan, SFR, Vidal, N, Poelmann, RE, Norman, JA 2008. Evolution of an arsenal: structural and functional diversification of the venom system in the advanced snakes (Caenophidia). Molecular & Cellular Proteomics 7, 215246.
Fujita, T 2002. Evolution of the lectin–complement pathway and its role in innate immunity. Nature Reviews Immunology 2, 346353.
Fuller, MF, McWilliam, R, Wang, TC, Giles, LR 1989. The optimum dietary amino acid pattern for growing pigs. 2. Requirements for maintenance and for tissue protein accretion. The British Journal of Nutrition 62, 255267.
Ganfornina, MD, Gutierrez, G, Bastiani, M, Sanchez, D 2000. A phylogenetic analysis of the lipocalin protein family. Molecular Biology and Evolution 17, 114126.
Ganfornina, MD, Sanchez, D, Greene, LH, Flower, DR 2006. The Lipocalin protein family: protein sequence, structure and relationship to the calycin superfamily. In Lipocalins (ed. B Akerstrom, N Borregaard, DR Flower and J-P Salier), pp. 1727. Landes Bioscience, Georgetown, TX.
Garattini, E, Mendel, R, Romão, MJ, Wright, R, Terao, M 2003. Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology. Biochemical Journal 372, 1532.
Gesase, AP, Satoh, Y 2003. Apocrine secretory mechanism: recent findings and unresolved problems. Histology and Histopathology 18, 597608.
Gregory, WK 1910. The orders of mammals. Bulletin of the American Museum of Natural History 27, 1524.
Griffiths, M 1978. Biology of the monotremes. Academic Press, New York, NY.
Gritli-Linde, A, Hallberg, K, Harfe, BD, Reyahi, A, Kannius-Janson, M, Nilsson, J, Cobourne, MT, Sharpe, PT, McMahon, AP, Linde, A 2007. Abnormal hair development and apparent follicular transformation to mammary gland in the absence of hedgehog signaling. Developmental Cell 12, 99112.
Hagiwara, K, Kikuchi, T, Endo, Y, Huqun, , Usui, K, Takahashi, M, Shibata, N, Kusakabe, T, Xin, H, Hoshi, S, Miki, M, Inooka, N, Tokue, Y, Nukiwa, T 2003. Mouse SWAM1 and SWAM2 are antibacterial proteins composed of a single whey acidic protein motif. Journal of Immunology 170, 19731979.
Hajjoubi, S, Rival-Gervier, S, Hayes, H, Floriot, S, Eggen, A, Piumi, F, Chardon, P, Houdebine, LM, Thepot, D 2006. Ruminants genome no longer contains whey acidic protein gene but only a pseudogene. Gene 370, 104112.
Hatsell, SJ, Cowin, P 2006. Gli3-mediated repression of Hedgehog targets is required for normal mammary development. Development 133, 36613670.
Hayssen, V, Blackburn, DG 1985. α-lactalbumin and the origins of lactation. Evolution 39, 11471149.
Hiemstra, PS 2002. Novel roles of protease inhibitors in infection and inflammation. Biochemical Society Transactions 30, 116120.
Hoffmann, JA, Kafatos, FC, Janeway, CA, Ezekowitz, RA 1999. Phylogenetic perspectives in innate immunity. Science 284, 13131318.
Hood, WR, Oftedal, OT, Kunz, TH 2011. Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 181, 423435.
Hopson, JA 1973. Endothermy, small size and the origin of mammalian reproduction. American Naturalist 107, 446452.
Horseman, ND, Buntin, JD 1995. Regulation of pigeon cropmilk secretion and parental behaviors by prolactin. Annual Review of Nutrition 15, 213238.
Jenssen, H, Hamill, P, Hancock, REW 2006. Peptide antimicrobial agents. Clinical Microbiology Reviews 19, 491511.
Jeong, J, Rao, AU, Xu, J, Ogg, SL, Hathout, Y, Fenselau, C, Mather, IH 2009. The PRY/SPRY/B30. 2 Domain of butyrophilin 1A1 (BTN1A1) binds to xanthine oxidoreductase. Journal of Biological Chemistry 284, 2244422456.
Jia, Y, Sun, Y, Wang, Z, Wang, Q, Wang, X, Zhao, X, Wang, J 2008. A single whey acidic protein domain (SWD)-containing peptide from fleshy prawn with antimicrobial and proteinase inhibitory activities. Aquaculture 284, 246259.
Kawasaki, K 2009. The SCPP gene repertoire in bony vertebrates and graded differences in mineralized tissues. Development Genes and Evolution 219, 147157.
Kawasaki, K, Weiss, KM 2003. Mineralized tissue and vertebrate evolution: the secretory calcium-binding phosphoprotein gene cluster. Proceedings of the National Academy of Sciences of the United States of America 100, 40604065.
Kawasaki, K, Lafont, A, Sire, J 2011. The evolution of milk casein genes from tooth genes before the origin of mammals. Molecular Biology and Evolution 28, 20532061.
Kemp, TS 2005. The origin and evolution of mammals. Oxford University Press, New York, NY.
Kontopidis, G, Holt, C, Sawyer, L 2004. Invited review: beta-lactoglobulin: binding properties, structure, and function. Journal of Dairy Science 87, 785796.
Konuma, T, Sakurai, K, Goto, Y 2007. Promiscuous binding of ligands by β-lactoglobulin involves hydrophobic interactions and plasticity. Journal of Molecular Biology 368, 209218.
Kupfer, A, Müller, H, Antoniazzi, MM, Jared, C, Greven, H, Nussbaum, RA, Wilkinson, M 2006. Parental investment by skin feeding in a caecilian amphibian. Nature 440, 926929.
Lefevre, CM, Sharp, JA, Nicholas, KR 2009. Characterisation of monotreme caseins reveals lineage-specific expansion of an ancestral casein locus in mammals. Reproduction, Fertility, and Development 21, 10151027.
Lefevre, CM, Sharp, JA, Nicholas, KR 2010. Evolution of lactation: ancient origin and extreme adaptations of the lactation system. Annual Review of Genomics and Human Genetics 11, 219238.
Lemay, DG, Lynn, DJ, Martin, WF, Neville, MC, Casey, TM, Rincon, G, Kriventseva, EV, Barris, WC, Hinrichs, AS, Molenaar, AJ, Pollard, KS, Maqbool, NJ, Singh, K, Murney, R, Zdobnov, EM, Tellam, RL, Medrano, JF, German, JB, Rijnkels, M 2009. The bovine lactation genome: insights into the evolution of mammalian milk. Genome Biology 10, R43. doi:10.1186/gb-2009-10-4-r43.
Lillywhite, HB 2006. Water relations of tetrapod integument. The Journal of Experimental Biology 209, 202226.
Lillywhite, HB, Mittal, AK, Garg, TK, Agrawal, N 1997. Integumentary structure and its relationship to wiping behaviour in the common Indian tree frog, Polypedates maculatus. Journal of Zoology 243, 675687.
Lourdais, O, Hoffman, TCM, Denardo, DF 2007. Maternal brooding in the children's python (Antaresia childreni) promotes egg water balance. Journal of Comparative physiology B: Biochemical, Systemic, and Environmental Physiology 177, 569577.
Lowe, JB, Varki, A 1999. Glycosyltransferases. In Essentials of glycobiology (ed. A Varki, R Cummings, J Esko, H Freeze, G Hart and J Marth), pp. 253266. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Luo, ZX, Crompton, AW, Sun, AL 2001. A new mammaliaform from the early Jurassic and evolution of mammalian characteristics. Science 292, 15351540.
Martin, HM, Hancock, JT, Salisbury, V, Harrison, R 2004. Role of xanthine oxidoreductase as an antimicrobial agent. Infection and Immunity 72, 49334939.
Mather, IH 2011. Milk lipids. Milk fat globule membrane. In Encyclopedia of dairy sciences (ed. J Fuquay, PF Fox and P McSweeney), vol. 3, 2nd edition, pp. 680690. Academic Press, San Diego.
Mather, IH, Keenan, TW 1998. Origin and secretion of milk lipids. Journal of Mammary Gland Biology and Neoplasia 3, 259273.
Mayer, JA, Foley, J, De La Cruz, D, Chuong, C-M, Widelitz, R 2008. Conversion of the nipple to hair-bearing epithelia by lowering bone morphogenetic protein pathway activity at the dermal–epidermal interface. The American Journal of Pathology 173, 13391348.
McClellan, HL, Miller, SJ, Hartmann, PE 2008. Evolution of lactation: nutrition v. protection with special reference to five mammalian species. Nutrition Research Reviews 21, 97116.
McManaman, JL, Reyland, ME, Thrower, EC 2006. Secretion and fluid transport mechanisms in the mammary gland: comparisons with the exocrine pancreas and the salivary gland. Journal of Mammary Gland Biology and Neoplasia 11, 249268.
McManaman, JL, Palmer, CA, Wright, RM, Neville, MC 2002. Functional regulation of xanthine oxidoreductase expression and localization in the mouse mammary gland: evidence of a role in lipid secretion. The Journal of Physiology 545, 567579.
Messer, M, Urashima, T 2002. Evolution of milk oligosaccharides and lactose. Trends in Glycoscience and Glycotechnology 14, 153176.
Nair, DG, Fry, BG, Alewood, P, Kumar, PP, Kini, RM 2007. Antimicrobial activity of omwaprin, a new member of the waprin family of snake venom proteins. The Biochemical Journal 402, 93104.
National Research Council 1995. Nutrient requirements of laboratory animals. National Academy Press, Washington, DC.
Nelson, CM, Bissell, MJ 2006. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annual Review of Cell and Developmental Biology 22, 287309.
Newburg, DS 1996. Oligosaccharides and glycoconjugates in human milk: their role in host defense. Journal of Mammary Gland Biology and Neoplasia 1, 271283.
Nicholas, KR, Messer, M, Elliott, C, Maher, F, Shaw, DC 1987. A novel whey protein synthesized only in late lactation by the mammary gland from the tammar (Macropus eugenii). The Biochemical Journal 241, 899904.
Nishino, T, Okamoto, K, Eger, BT, Pai, EF, Nishino, T 2008. Mammalian xanthine oxidoreductase – mechanism of transition from xanthine dehydrogenase to xanthine oxidase. The FEBS Journal 275, 32783289.
Novacek, MJ, Rougier, GW, Wible, JR, McKenna, MC, Dashzeveg, D, Horovitz, I 1997. Epipubic bones in eutherian mammals from the Late Cretaceous of Mongolia. Nature 389, 483486.
Oftedal, OT 1997. Lactation in whales and dolphins: evidence of divergence between baleen- and toothed-species. Journal of Mammary Gland Biology and Neoplasia 2, 205230.
Oftedal, OT 2000. Use of maternal reserves as a lactation strategy in large mammals. Proceedings of the Nutrition Society 59, 99106.
Oftedal, OT 2002a. The origin of lactation as a water source for parchment-shelled eggs. Journal of Mammary Gland Biology and Neoplasia 7, 253266.
Oftedal, OT 2002b. The mammary gland and its origin during synapsid evolution. Journal of Mammary Gland Biology and Neoplasia 7, 225252.
Oftedal, OT 2011. Milk of marine mammals. In Encyclopedia of dairy sciences (ed. J Fuquay, PF Fox and P McSweeney), vol. 3, 2nd edition, pp. 563580. Academic Press, San Diego, CA.
Oftedal, OT, Gittleman, JL 1989. Patterns of energy output during reproduction in carnivores. In Carnivore behavior, ecology and evolution (ed. JL Gittleman), pp. 355378. Cornell University Press, Ithaca, NY.
Oftedal, OT, Iverson, SJ 1995. Comparative analysis of non-human milks. A. phylogenetic variation in the gross composition of milks. In Handbook of milk composition (ed. RG Jensen), pp. 749789. Academic Press, San Diego, CA.
Oftedal, OT, Boness, DJ, Tedman, RA 1987a. The behavior, physiology, and anatomy of lactation in the Pinnipedia. Current Mammalogy 1, 175245.
Oftedal, OT, Iverson, SJ, Boness, DJ 1987b. Milk and energy intakes of suckling California sea lion Zalophus californianus pups in relation to sex, growth, and predicted maintenance requirements. Physiological Zoology 60, 560575.
Oftedal, OT, Bowen, DW, Boness, DJ 1993a. Energy transfer by lactating hooded seals and nutrient deposition in their pups during the 4 days from birth to weaning. Physiological Zoology 66, 412436.
Oftedal, OT, Alt, GL, Widdowson, EM, Jakubasz, MR 1993b. Nutrition and growth of suckling black bears (Ursus americanus) during their mothers’ winter fast. British Journal of Nutrition 70, 5979.
Ogg, SL, Weldon, AK, Dobbie, L, Smith, AJH, Mather, IH 2004. Expression of butyrophilin (Btn1a1) in lactating mammary gland is essential for the regulated secretion of milk-lipid droplets. Proceedings of the National Academy of Sciences of the United States of America 101, 1008410089.
Packard, MJ, Seymour, RS 1997. Evolution of the amniote egg. In Amniote origins: completing the transition to land (ed. SS Sumida and KLM Martin), pp. 265290. Academic Press, San Diego, CA.
Perez, MD, Calvo, M 1995. Interaction of beta-lactoglobulin with retinol and fatty acids and its role as a possible biological function for this protein: a review. Journal of Dairy Science 78, 978988.
Pervaiz, S, Brew, K 1985. Homology of β-lactoglobulin, serum retinol-binding protein, and protein HC. Science 228, 335337.
Piotte, CP, Grigor, MR 1996. A novel marsupial protein expressed by the mammary gland only during the early lactation and related to the Kunitz proteinase inhibitors. Archives of Biochemistry and Biophysics 330, 5964.
Piotte, CP, Hunter, AK, Marshall, CJ, Grigor, MR 1998. Phylogenetic analysis of three lipocalin-like proteins present in the milk of Trichosurus vulpecula (Phalangeridae, Marsupialia). Journal of Molecular Evolution 46, 361369.
Pond, CM 1977. The significance of lactation in the evolution of mammals. Evolution 31, 177199.
Prager, EM, Wilson, AC 1988. Ancient origin of lactalbumin from lysozyme: analysis of DNA and amino acid sequences. Journal of Molecular Evolution 27, 326335.
Qasba, PK, Kumar, S 1997. Molecular divergence of lysozymes and α-lactalbumin. Critical Reviews in Biochemistry and Molecular Biology 32, 255306.
Quagliata, S, Malentacchi, C, Delfino, C, Brunasso, AMG, Delfino, G 2006. Adaptive evolution of secretory cell lines in vertebrate skin. Caryologia 59, 187206.
Ramakrishnan, B, Qasba, PK 2001. Crystal structure of lactose synthase reveals a large conformational change in its catalytic component, the β-1,4-galactosyltransferase-I. Journal of Molecular Biology 310, 205218.
Ranganathan, S, Simpson, KJ, Shaw, DC, Nicholas, KR 1999. The whey acidic protein family: a new signature motif and three-dimensional structure by comparative modeling. Journal of Molecular Graphics & Modelling 17, 106113, 134–136.
Reeves, PG, Nielsen, FH, Fahey, GC 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. The Journal of Nutrition 123, 19391951.
Reich, C, Arnould, J 2007. Evolution of Pinnipedia lactation strategies: a potential role for α-lactalbumin? Biology Letters 3, 546549.
Reilly, SM, White, TD 2003. Hypaxial motor patterns and the function of epipubic bones in primitive mammals. Science 299, 400402.
Rhodes, DA, Stammers, M, Malcherek, G, Beck, S, Trowsdale, J 2001. The cluster of BTN genes in the extended major histocompatibility complex. Genomics 71, 351362.
Rijnkels, M 2002. Multispecies comparison of the casein gene loci and evolution of casein gene family. Journal of Mammary Gland Biology and Neoplasia 7, 327345.
Rijnkels, M 2003. Multispecies comparative analysis of a mammalian-specific genomic domain encoding secretory proteins. Genomics 82, 417432.
Robinson, GW 2004. Identification of signaling pathways in early mammary gland development by mouse genetics. Breast Cancer Research 6, 105108.
Sanchez, D, Ganfornina, MD, Gutierrez, G, Marin, A 2003. Exon–intron structure and evolution of the Lipocalin gene family. Molecular Biology and Evolution 20, 775783.
Sanchez, D, Ganfornina, MD, Gutierrez, G, Gauthier-Jauneau, A-C, Risler, J-L, Salier, J-P 2006. Lipocalin genes and their evolutionary history. In Lipocalins (ed. B Akerstrom, N Borregaard, DR Flower and J-P Salier), pp. 516. Landes Bioscience, Georgetown, TX.
Sawyer, L 2003. β-lactoglobulin. In Advanced dairy chemistry – I. Proteins. Part A (ed. PF Fox and P McSweeney), pp. 319386. Kluwer Academic, New York, NY.
Senda, A, Hatakeyama, E, Kobayashi, R, Fukuda, K, Uemura, Y, Saito, T, Packer, C, Oftedal, OT, Urashima, T 2010. Chemical characterization of milk oligosaccharides of an African lion (Panthera leo) and a clouded leopard (Neofelis nebulosa). Animal Science Journal 81, 687693.
Shaper, NL, Charron, M, Lo, NW, Shaper, JH 1998. β-1,4-galactosyltransferase and lactose biosynthesis: recruitment of a housekeeping gene from the nonmammalian vertebrate gene pool for a mammary gland specific function. Journal of Mammary Gland Biology and Neoplasia 3, 315324.
Sharp, JA, Lefevre, C, Nicholas, KR 2007. Molecular evolution of monotreme and marsupial whey acidic protein genes. Evolution & Development 9, 378392.
Sharp, JA, Lefevre, C, Nicholas, KR 2008. Lack of functional alpha-lactalbumin prevents involution in Cape fur seals and identifies the protein as an apoptotic milk factor in mammary gland involution. BMC Biology 6, 48. doi:10.1186/1741-7007-6-48.
Sharp, JA, Cane, KN, Lefevre, C, Arnould, JPY, Nicholas, KR 2005. Fur seal adaptations to lactation: insights into mammary gland function. Current Topics in Developmental Biology 72, 275308.
Shennan, DB, Peaker, M 2000. Transport of milk constituents by the mammary gland. Physiological Reviews 80, 925951.
Sidor, CA, Hopson, JA 1998. Ghost lineages and “mammalness”: assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24, 254273.
Smith, IA, Knezevic, BR, Ammann, JU, Rhodes, DA, Aw, D, Palmer, DB, Mather, IH, Trowsdale, J 2010a. BTN1A1, the mammary gland butyrophilin, and BTN2A2 are both inhibitors of T cell activation. The Journal of Immunology 184, 35143525.
Smith, VJ, Desbois, AP, Dyrynda, EA 2010b. Conventional and unconventional antimicrobials from fish, marine invertebrates and micro-algae. Marine Drugs 8, 12131262.
Smolenski, G, Haines, S, Fiona, YSK, Bond, J, Farr, V, Davis, SR, Stelwagen, K, Wheeler, TT 2007. Characterisation of host defence proteins in milk using a proteomic approach. Journal of Proteome Research 6, 207215.
Smyth, E, Clegg, RA, Holt, C 2004. A biological perspective on the structure and function of caseins and casein micelles. International Journal of Dairy Technology 57, 121126.
Stacey, A, Schnieke, A, Kerr, M, Scott, A, McKee, C, Cottingham, I, Binas, B, Wilde, C, Colman, A 1995. Lactation is disrupted by α-lactalbumin deficiency and can be restored by human α-lactalbumin gene replacement in mice. Proceedings of the National Academy of Sciences of the United States of America 92, 28352839.
Starck, JM, Ricklefs, R 1998. Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, New York, NY.
Stinnakre, MG, Vilotte, JL, Soulier, S, Mercier, JC 1994. Creation and phenotypic analysis of alpha-lactalbumin-deficient mice. Proceedings of the National Academy of Sciences of the United States of America 91, 65446548.
Stoeckelhuber, M, Stoeckelhuber, BM, Welsch, U 2003. Human glands of Moll: histochemical and ultrastructural characterization of the glands of Moll in the human eyelid. Journal of Investigative Dermatology 121, 2836.
Stoeckelhuber, M, Schubert, C, Kesting, MR, Loeffelbein, DJ, Nieberler, M, Koehler, C, Welsch, U 2011. Human axillary apocrine glands: proteins involved in the apocrine secretory mechanism. Histology and Histopathology 26, 177184.
Stoeckelhuber, M, Matthias, C, Andratschke, M, Stoeckelhuber, BM, Koehler, C, Herzmann, S, Sulz, A, Welsch, U 2006. Human ceruminous gland: ultrastructure and histochemical analysis of antimicrobial and cytoskeletal components. The Anatomical Record Part A: Discoveries in Molecular, Cellular, and Evolutionary Biology 288A, 877884.
Taigen, TL, Pough, FH, Stewart, MM 1984. Water balance of terrestrial anuran (Eleutherodactylus coqui) eggs: importance of parental care. Ecology 65, 248255.
Thomas, B, Gruca, LL, Bennett, C, Parimi, PS 2008. Metabolism of methionine in the newborn infant: response to the parenteral and enteral administration of nutrients. Pediatric Research 64, 381386.
Thompson, MB, Biazik, JB, Lui, S, Adams, SM, Murphy, CR 2006. Morphological and functional changes to the uterus of lizards with different placental complexities. Herpetological Monographs 20, 178185.
Toba, T, Nagashima, S, Adachi, S 1991. Is lactose really present in plants? Journal of the Science of Food and Agriculture 54, 305308.
Topcic, D, Auguste, A, De Leo, AA, Lefevre, C, Digby, MR, Nicholas, KR 2009. Characterization of the tammar wallaby (Macropus eugenii) whey acidic protein gene; new insights into the function of the protein. Evolution & Development 11, 363375.
Treccani, L, Mann, K, Heinemann, F, Fritz, M 2006. Perlwapin, an abalone nacre protein with three four-disulfide core (whey acidic protein) domains, inhibits the growth of calcium carbonate crystals. Biophysical Journal 91, 26012608.
Triplett, AA, Sakamoto, K, Matulka, LA, Shen, L, Smith, GH, Wagner, KU 2005. Expression of the whey acidic protein (Wap) is necessary for adequate nourishment of the offspring but not functional differentiation of mammary epithelial cells. Genesis 43, 111.
Tyndale-Biscoe, H, Renfree, M 1987. Reproductive physiology of marsupials. Cambridge University Press, Cambridge, UK.
Uemura, Y, Takahashi, S, Senda, A, Fukuda, K, Saito, T, Oftedal, OT, Urashima, T 2009. Chemical characterization of milk oligosaccharides of a spotted hyena (Crocuta crocuta). Comparative Biochemistry and Physiology A: Molecular & Integrative Physiology 152, 158161.
Urashima, T, Saito, T, Nakamura, T, Messer, M 2001. Oligosaccharides of milk and colostrum in non-human mammals. Glycoconjugate Journal 18, 357371.
Varki, A 1998. Factors controlling the glycosylation potential of the Golgi apparatus. Trends in Cell Biology 8, 3440.
Vorbach, C 2003. Xanthine oxidoreductase is central to the evolution and function of the innate immune system. Trends in Immunology 24, 512517.
Vorbach, C, Scriven, A, Capecchi, MR 2002. The housekeeping gene xanthine oxidoreductase is necessary for milk fat droplet enveloping and secretion: gene sharing in the lactating mammary gland. Genes & Development 16, 32233235.
Vorbach, C, Capecchi, MR, Penninger, JM 2006. Evolution of the mammary gland from the innate immune system? BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology 28, 606616.
Watson, CJ, Khaled, WT 2008. Mammary development in the embryo and adult: a journey of morphogenesis and commitment. Development 135, 9951003.
West, KL, Oftedal, OT, Carpenter, JR, Krames, BJ, Campbell, M, Sweeney, JC 2007. Effect of lactation stage and concurrent pregnancy on milk composition in the bottlenose dolphin. Journal of Zoology 273, 148160.
Yang, MC, Chen, NC, Chen, C-J, Wu, CY, Mao, SJT 2009. Evidence for beta-lactoglobulin involvement in vitamin D transport in vivo – role of the gamma-turn (Leu-Pro-Met) of beta-lactoglobulin in vitamin D binding. FEBS Journal 276, 22512265.
Zhang, Z, Zhang, B, Nie, X, Liu, Q, Xie, F, Shang, D 2009. Transcriptome analysis and identification of genes related to immune function in skin of the Chinese brown frog. Zoological Science 26, 8086.
Zhao, Y, Jin, Y, Lee, W, Zhang, Y 2006. Purification of a lysozyme from skin secretions of Bufo andrewsi. Comparative Biochemistry and Physiology C: Toxicology & Pharmacology 142, 4652.
Zou, Z, Evans, JD, Lu, Z, Zhao, P, Williams, M, Sumathipala, N, Hetru, C, Hultmark, D, Jiang, H 2007. Comparative genomic analysis of the Tribolium immune system. Genome Biology 8, R177. doi:10.1186/gb-2007-8-8-r177.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

  • ISSN: 1751-7311
  • EISSN: 1751-732X
  • URL: /core/journals/animal
Please enter your name
Please enter a valid email address
Who would you like to send this to? *



Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed