Evolution of Lactation: Ancient Origin and Extreme Adaptations of the Lactation System

Lefèvre, Christophe; Sharp, Julie A.; Nicholas, Kevin R.

doi:10.1146/annurev-genom-082509-141806

Cited by 140 publications

(114 citation statements)

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“…The proposal that mammary secretion has an ancient origin and long evolutionary history (Oftedal, 2002a and2002b) is increasingly accepted, especially in the face of supportive molecular evidence (Kawasaki and Weiss, 2003;Vorbach et al, 2006;Brawand et al, 2008;McClellan et al, 2008;Capuco and Akers, 2009;Lemay et al, 2009;Lefevre et al, 2010;Kawasaki et al, 2011). It is now possible to formulate a more detailed scenario by which the secreted fluid came to resemble in form and function what we now know as milk.…”

Section: Resultsmentioning

confidence: 99%

“…Lactation is highly complex and apparently of ancient evolutionary origin (Oftedal, 2002b;Lefevre et al, 2010). The detailed signaling crosstalk among epithelial and underlying mesenchyme cells that is required for the differentiation, ductal branching, and proliferation of mammary tissue is only now being unraveled (Watson and Khaled, 2008), and the functional significance and patterns of expression of thousands of mammary genes are under investigation (Lemay et al, 2009).…”

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The evolution of milk secretion and its ancient origins

Oftedal

2012

Animal

196

142

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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 a-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 b-lactoglobulin and whey acidic protein, which with a-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.Keywords: evolution, lactation, milk composition, casein, milk fat globule ImplicationsLactation has an evolutionary origin and biological context within which its secretory processes and milk constituents evolved. This revi...

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Section: Resultsmentioning

confidence: 99%

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The evolution of milk secretion and its ancient origins

Oftedal

2012

Animal

196

142

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“…They are highly specialized skin appendages that allow for extensive postnatal care of the progeny by providing a primary source of nutrition and immune protection (25,26). Their early development depends on complex epithelial-mesenchyme interactions (27,28), starting with the formation of the mammary lines, a thickening of the ectoderm on the lateral sides of the embryo stretching between the forelimbs and hind limbs.…”

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confidence: 99%

Control of Hoxd gene transcription in the mammary bud by hijacking a preexisting regulatory landscape

Schep

Necşulea

Rodríguez-Carballo

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Vertebrate Hox genes encode transcription factors operating during the development of multiple organs and structures. However, the evolutionary mechanism underlying this remarkable pleiotropy remains to be fully understood. Here, we show that Hoxd8 and Hoxd9, two genes of the HoxD complex, are transcribed during mammary bud (MB) development. However, unlike in other developmental contexts, their coexpression does not rely on the same regulatory mechanism. Hoxd8 is regulated by the combined activity of closely located sequences and the most distant telomeric gene desert. On the other hand, Hoxd9 is controlled by an enhancer-rich region that is also located within the telomeric gene desert but has no impact on Hoxd8 transcription, thus constituting an exception to the global regulatory logic systematically observed at this locus. The latter DNA region is also involved in Hoxd gene regulation in other contexts and strongly interacts with Hoxd9 in all tissues analyzed thus far, indicating that its regulatory activity was already operational before the appearance of mammary glands. Within this DNA region and neighboring a strong limb enhancer, we identified a short sequence conserved in therian mammals and capable of enhancer activity in the MBs. We propose that Hoxd gene regulation in embryonic MBs evolved by hijacking a preexisting regulatory landscape that was already at work before the emergence of mammals in structures such as the limbs or the intestinal tract.enhancers | TAD | mammalian development | mammary gland

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“…And, bizarrely, her teats can function independently, with each baby wallaby effectively stuck to one teat for the first 200 days in the pouch. In fact, a joey may have a pouch mate of a different age that feeds on an adjacent teat -and which receives milk of a different composition, appropriate for its age 1 .…”

mentioning

confidence: 99%

Development: Mother's milk: A rich opportunity

Petherick

2010

Nature

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Evolution of Lactation: Ancient Origin and Extreme Adaptations of the Lactation System

Cited by 140 publications

References 93 publications

The evolution of milk secretion and its ancient origins

The evolution of milk secretion and its ancient origins

Control of Hoxd gene transcription in the mammary bud by hijacking a preexisting regulatory landscape

Development: Mother's milk: A rich opportunity

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