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Origin and Evolution of the Major Constituents of Milk

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Advanced Dairy Chemistry

Abstract

Accumulating evidence indicates that the evolutionary novelty known as milk, and its constituents, is of ancient origin, dating back 300+ million years. Milk may derive from the secretion of apocrine-like skin glands that produced water- and antimicrobial-rich fluids of benefit to attended eggs. The casein micelle evolved from much simpler secretory calcium-binding phosphoproteins. The milk fat globule evolved by co-opting membrane (butyrophilin), cytosol (xanthine oxidoreductase), and intracellular lipid droplet (adipophilin) proteins of secretory cells into new or expanded functions. Milk sugar secretion required structural and functional modification of a secreted antibacterial protein into a Golgi regulatory protein (α-lactalbumin). Other whey proteins (β-lactoglobulin, whey acidic protein) apparently lost prior functions in becoming nutrient sources for suckling young.

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Acknowledgements

I am grateful to Cambridge University Press for permission to reprint text from my earlier review (Oftedal, 2012) in the journal Animal(© 2011 The Animal Consortium) and to the American Association for the Advancement of Science, the American Museum of Natural History, Elsevier B.V., Johns Hopkins University Press, Jonathan Kingdon, Landes Bioscience, Oxford University Press, the Royal Society, the Society for Sedimentary Geology, Springer Science and Business Media, the University of Tennessee Department of Earth and Planetary Sciences and Yale Scientific Magazine for permission to reproduce copyrighted figures in this paper. I especially thank Alexander Kupfer for kindly providing original photographs of skin feeding in caecilians and Pradman Qasba for providing a corrected version of a figure. I also thank many colleagues for stimulating discussion on the evolution of milk and lactation, a topic which was still in a primitive state when I first presented my ideas at a Gordon Research Conference on Mammary Gland Biology in New Hampshire in June 1999. Although the relationship of α-lactalbumin to lysozyme had long been known, the origin of the caseins was a great mystery, and Ian Mather had yet to clarify for me some of the concerns with an “apocrine origin” for milk fat secretion. Thanks to molecular genetics, there have been great strides in understanding the origin and evolution of the genes required for milk protein synthesis, none of which I can claim credit for. I am especially grateful for the ideas and input of Regina Eisert, Geoff Birchard, Murray Grigor, Peter Hartmann, Michael Messer, Kevin Nicholas, Peggy Neville, Ian Mather, Monique Rijnkels, Tadasu Urashima, and Elsie Widdowson. The Smithsonian Environmental Research Center and its director, Tuck Hines, have supported my long forays into lactation research, even though my current program is focused on nutritional ecology. I thank the Smithsonian Institution Library and its staff for assistance in obtaining the wide range of research publications needed for a review of this type.

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  1. Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA

    O. T. Oftedal

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  1. O. T. Oftedal
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Correspondence to O. T. Oftedal .

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  1. School of Food and Nutritional Sciences, University College Cork, Cork, College Ro, Ireland

    Paul L. H. McSweeney

  2. Fac. Food Technology & Nutrition, Dept. Food Science, University College Cork, Cork, Ireland

    Patrick F. Fox

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Oftedal, O.T. (2013). Origin and Evolution of the Major Constituents of Milk. In: McSweeney, P., Fox, P. (eds) Advanced Dairy Chemistry. Springer, Boston, MA. https://doi.org/10.1007/978-1-4614-4714-6_1

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