The Behavior, Physiology, and Anatomy of Lactation in the Pinnipedia

Oftedal, Olav T.; Boness, Daryl J.; Tedman, Raymond

doi:10.1007/978-1-4757-9909-5_6

Cited by 250 publications

(182 citation statements)

References 121 publications

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“…The evolution of the placenta in eutherians also removed much of the need for nutrient transfer during early development. Marsupials, which have no or very simple placentas, rely on lactation for a greater span of development than eutherians, and not surprisingly, marsupial milks undergo much greater changes in composition over the course of lactation than do most eutherian milks (Oftedal and Iverson, 1995). It is not known whether some of the unique whey proteins that have been found in marsupials represent milk constituents that were lost during eutherian evolution, or if they have evolved since marsupials and eutherians diverged.…”

Section: Resultsmentioning

confidence: 99%

“…The Milk fat globule (MFG) Mammals vary tremendously in the fat content of their milk (from less than 1% in rhinos and some lemurs to 60% in some seals; Oftedal and Iverson, 1995); however, in all species studied, milk lipids are secreted as specialized structures known as MFGs. MFGs are lipid spheres bounded sequentially by a phospholipid monolayer, an inner protein coat, a bilayered phospholipid membrane, and a glycosylated surface (Mather and Keenan, 1998).…”

Section: Caseinsmentioning

confidence: 99%

“…Milk sugar synthesis All mammalian milks contain at least traces of sugar (Oftedal and Iverson, 1995); in most eutherians the predominant sugar is lactose, whereas in monotremes, marsupials and some eutherian carnivores oligosaccharides predominate (Urashima et al, 2001;Messer and Urashima, 2002;Uemura et al, 2009;Senda et al, 2010). Both lactose and oligosaccharides with lactose at the reducing end are unique to milk (Toba et al, 1991) and require a novel synthetic pathway.…”

Section: Evolution Of Milk Secretionmentioning

confidence: 99%

“…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). Secreted milk is extremely varied in composition -from trace levels of fat in rhinos to more than 60% fat in some ice-breeding seals (Oftedal and Iverson, 1995) -and contains unique proteins (a-, b-, and k-caseins, b-lactoglobulin, a-lactalbumin, whey acidic protein (WAP)), membrane-enclosed lipid droplets, and sugars (lactose, milk oligosaccharides) that are not found elsewhere in nature.…”

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confidence: 99%

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The evolution of milk secretion and its ancient origins

Oftedal

2012

Animal

203

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%

Section: Caseinsmentioning

confidence: 99%

Section: Evolution Of Milk Secretionmentioning

confidence: 99%

mentioning

confidence: 99%

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The evolution of milk secretion and its ancient origins

Oftedal

2012

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“…Milk lipids of seals and sea lions furnish 85-95% of the total caloric intake of neonates and are characterized primarily by long-chain and unsaturated fatty acids, including a very large percentage (10-30%) of n-3 PUFA derived from their marine diets (28,29). Suckling pups consume phenomenal quantities of lipid daily at 600 g to 5 kg (30,31), or up to 10-to 20-fold higher on a body weight basis than neonates of the human or dog. Rapid blubber deposition suggests rapid and efficient absorption of milk lipid (28,32,33), but the mechanisms of hydrolysis and digestion are unknown.…”

mentioning

confidence: 99%

Positional specificity of gastric hydrolysis of long‐chain n−3 polyunsaturated fatty acids of seal milk triglycerides

Iverson

Sampugna

Oftedal

1992

Lipids

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Long-chain n-3 polyunsaturated fatty acids (n-3 PUFA) of marine oils are important dietary components for both infants and adults, and are incorporated into mlUo~ following maternal dietary intake. However, little is known about the hydrolysis of these PUFA from milk triglycerides (TG) by lipases in suckling young. Seals, like human~, possess gastric lipase; however, the milk lipids of seals and sea lions are almost devoid of the readily hydrolyzable medium,chain fatty acids, and are characterized by a large percentage (10-30%) of n-3 PUFA. Gastric hydrolysis of milk lipids was studied in vivo in suckling pups of three species (the California sea lion, the harp seal and the hooded seal) in order to elucidate the actions and specifit~ ity of gastric lipases on milk TG in relation to fatty acid composition and TG structure. Regardless of milk fat content (31-61% fat) or extent of gastric hydrolysis (10-56%), the same fatty acids were preferentially released in all three species, as determined by their relative enrichment in the free fatty acid (FFA) fraction. In addition to 16:1 and 18:0, these were the PUFA of 18 carbons and longer, except for 22:6n-3. Levels of 20:5n-3 were most notably enriched in FFA, at up to five times that found in the TG. Although 22:6n-3 was apparently also released from the TG (reduced in the diglyceride), it was also notably re~ duced in FFA. Positional analysis of milk TG based on the products of Grignard hydrolysis revealed that these PUFA, including 22:6n-3, were preferentially esterified at the a-position of the TG, and that the fatty acids not released during gastric hydrolysis were located at the sn-2 position. The extreme reduction of 22:6n~ and enrichment of 20:5n-3 in FFA is discussed. Results from this study are consistent with reports that gastric lipase acts stere~ specifically to release fatty acids at the a-positions (sn-3, sn-1). We conclude that the n-3 PUFA in milk are efficiently hydrolyzed by gastric lipase and that this has important implications for digestion of milks enriched in PUFA by neonates in general. Lipids 27, 870-878 (1992).Long-chain n-3 polyunsaturated fatty acids (n-3 PUFA), characteristic of marine otis, have become a major focus of research due to their potent

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Milk composition reflects pattern of material care in prosimian primates

1997

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Hypothesized relationships between milk composition and life history traits were examined by analyzing mid‐lactation milks of seven lemurs (Eulemur fulvus, E. macaco, E. rubriventer, E. mongoz, Varecia variegata, Hapalemur griseus, Lemur catta), three bushbabies (Otolemur crassicaudatus, O. garnettii, Galago moholi), and two lorises (Nycticebus coucang, Loris tardigradus); partial data were also obtained for the lemuroid Cheirogaleus medius. There were significant differences in milk composition among species within either Eulemur or Otolemur, but the four genera for which multiple samples were available (Eulemur, Varecia, Otolemur, and Nycticebus) exhibited large composition differences. Eulemur milk was, on average, very dilute (9.9% dry matter) and low in energy (0.49 kcal/g). These milks contained 0.9% fat, 1.2% protein, and 8.4% carbohydrate on a fresh weight basis. Protein energy comprised only about 15% of total milk energy. Varecia had significantly higher dry matter (13.5%), fat (3.2%), protein (4.2%), gross energy (0.80 kcal/g), and protein energy: total energy ratio (28%) than Eulemur. Milks of the lorisoid genera Otolemur and Nycticebus were very similar, and both had significantly higher dry matter (18.3, 16.3%), fat (7.6, 7.0%), and gross energy concentration (1.27, 1.13 kcal/g) than either lemuroid genus. Otolemur milk was higher in protein than Nycticebus milk. We conclude that lorises, bushbabies, and perhaps cheirogaleids produce relatively rich, energy‐dense milks in comparison with anthropoid primates. However, dilute milks appear to be uniformly found among species of Eulemur and perhaps in Lemur catta. The milk of Varecia (and perhaps Hapalemur) is intermediate in composition. Differences in milk composition among prosimians may be related to differences in maternal care: prosimians that carry their young during lactation produce more dilute milks than do species which leave their young unattended for prolonged periods. When looking at primates as a whole, however, the picture is somewhat less clear, since the milks of some “parkers” like Varecia do closely resemble those of large anthropoid primates who carry their young. Am. J. Primatol. 41:195–211, 1997. © 1997 Wiley‐Liss, Inc.

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The Behavior, Physiology, and Anatomy of Lactation in the Pinnipedia

Cited by 250 publications

References 121 publications

The evolution of milk secretion and its ancient origins

The evolution of milk secretion and its ancient origins

Positional specificity of gastric hydrolysis of long‐chain n−3 polyunsaturated fatty acids of seal milk triglycerides

Milk composition reflects pattern of material care in prosimian primates

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