The Evolution of Lactation in Mammalian Species.

Lactation is a defining characteristic of all mammals, and, indeed, mammals draw their name from mammae, or mammary glands. The evolution of mammary glands has been the subject of debate since Charles Darwin. The purpose of this brief review is not to examine all past theories of mammary evolution but to consider the evolution of the mammary gland in relation to (1) modern paleobiology, giving special attention to the mammaliaforms which had many mammalian features, including delayed tooth development suggestive of milk intake.

Chemical structures of oligosaccharides in milks of the American black bear (Ursus americanus americanus) and cheetah (Acinonyx jubatus).

The milk oligosaccharides were studied for two species of the Carnivora: the American black bear (Ursus americanus, family Ursidae, Caniformia), and the cheetah, (Acinonyx jubatus, family Felidae, Feliformia). Lactose was the most dominant saccharide in cheetah milk, while this was a minor saccharide and milk oligosaccharides predominated over lactose in American black bear milk. The structures of 8 neutral saccharides from American black bear milk were found to be Gal(β1-4)Glc (lactose), Fuc(α1-2)Gal(β1-4)Glc (2'-fucosyllactose), Gal(α1-3)Gal(β1-4)Glc (isoglobotriose), Gal(α1-3)[Fuc(α1-2)]Gal(β1-4)Glc (B-tetrasaccharide), Gal(α1-3)[Fuc(α1-2)]Gal(β1-4)[Fuc(α1-3)]Glc (B-pentasaccharide), Fuc(α1-2)Gal(β1-4)[Fuc(α1-3)]GlcNAc(β1-3)Gal(β1-4)Glc (difucosyl lacto-N-neotetraose), Gal(α1-3)Gal(β1-4)[Fuc(α1-3)]GlcNAc(β1-3)Gal(β1-4)Glc (monogalactosyl monofucosyl lacto-N-neotetraose) and Gal(α1-3)Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (Galili pentasaccharide).

Getting to the root of scales, feather and hair: As deep as odontodes?

While every jawed vertebrate, or its recent ancestor, possesses teeth, skin appendages are characteristic of the living clades: skin denticles (odontodes) in chondrichthyans, dermal scales in teleosts, ducted multicellular glands in amphibians, epidermal scales in squamates, feathers in birds and hair-gland complexes in mammals, all of them showing a dense periodic patterning. While the odontode origin of teleost scales is generally accepted, the origin of both feather and hair is still debated. They appear long before mammals and birds, at least in the Jurassic in mammaliaforms and in ornithodires (pterosaurs and dinosaurs), and are contemporary to scales of early squamates.

4-O-Acetyl-sialic acid (Neu4,5Ac2) in acidic milk oligosaccharides of the platypus (Ornithorhynchus anatinus) and its evolutionary significance.

Monotremes (echidnas and platypus) retain an ancestral form of reproduction: egg-laying followed by secretion of milk onto skin and hair in a mammary patch, in the absence of nipples. Offspring are highly immature at hatching and depend on oligosaccharide-rich milk for many months. The primary saccharide in long-beaked echidna milk is an acidic trisaccharide Neu4,5Ac2(α2-3)Gal(β1-4)Glc (4-O-acetyl 3'-sialyllactose), but acidic oligosaccharides have not been characterized in platypus milk.

Perfluoroalkyl substances detected in the world's southernmost marine mammal, the Weddell seal (Leptonychotes weddellii).

This study investigates concentrations of 18 perfluoroalkyl substances (PFAS) in blood plasma of adult lactating Weddell seals (Leptonychotes weddellii) (n = 10) from McMurdo Sound, Antarctica. Perfluoroundecanoic acid (PFUnDA) was detected in all samples at concentrations ranging from 0.08 to 0.

Proximate composition of milk of the bongo (Tragelaphus eurycerus) in comparison to other African bovids and to hand-rearing formulas.

African bovids represent a highly diverse group with divergent neonatal care strategies. The extent to which their milks reflect this diversity is poorly understood. We analyzed milk of the bongo (Tragelaphus eurycerus) to compare its composition to milks of other African bovids and to evaluate bongo milk replacement formulas.

Can an ancestral condition for milk oligosaccharides be determined? Evidence from the Tasmanian echidna (Tachyglossus aculeatus setosus).

The monotreme pattern of egg-incubation followed by extended lactation represents the ancestral mammalian reproductive condition, suggesting that monotreme milk may include saccharides of an ancestral type. Saccharides were characterized from milk of the Tasmanian echidna Tachyglossus aculeatus setosus. Oligosaccharides in pooled milk from late lactation were purified by gel filtration and high-performance liquid chromatography using a porous graphitized carbon column and characterized by (1)H NMR spectroscopy; oligosaccharides in smaller samples from early and mid-lactation were separated by ultra-performance liquid chromatography and characterized by negative electrospray ionization mass spectrometry (ESI-MS) and tandem collision mass spectroscopy (MS/MS) product ion patterns.

Evo-devo of the mammary gland.

We propose a new scenario for mammary evolution based on comparative review of early mammary development among mammals. Mammary development proceeds through homologous phases across taxa, but evolutionary modifications in early development produce different final morphologies. In monotremes, the mammary placode spreads out to form a plate-like mammary bulb from which more than 100 primary sprouts descend into mesenchyme.

Neutral and acidic milk oligosaccharides of the striped skunk (Mephitidae: Mephitis mephitis).

The biological significance of the tremendous variation in proportions of oligosaccharides and lactose among mammalian milks is poorly understood. We investigated milk oligosaccharides of the striped skunk (Mephitis mephitis) and compared these results to other species of the clade Mustelida. Individual oligosaccharides were identified by proton nuclear magnetic resonance spectroscopy.

Daughter dearest: Sex-biased calcium in mother's milk among rhesus macaques.

Mother's milk provides building blocks necessary for infant development and growth postnatally. Minerals in milk are particularly important for infant skeletal development and may reflect maternal characteristics that are associated with the capacity to synthesize milk and sex-specific developmental priorities of the infant. Using a large sample of mother-infant dyads assigned to the outdoor breeding colony at the California National Primate Research Center (N=104), we investigated the relationship of milk calcium (Ca) and phosphorus (P) concentrations and the ratio of Ca/P to maternal and infant characteristics and to other milk variables.

Milk composition in the Weddell seal Leptonychotes weddellii: evidence for a functional role of milk carbohydrates in pinnipeds.

We propose that secretion of milk sugar has important consequences for the metabolic economies of lactating phocid seals and their pups. Milk was collected from 21 Weddell seals Leptonychotes weddellii in McMurdo Sound, Antarctica, and assayed by standard methods. Milk composition changed over the course of lactation, but at mid- to late lactation (16-40 d postpartum), Weddell seal milk composition was relatively constant at 33.

Variation in the composition of milk of Asian elephants (Elephas maximus) throughout lactation.

We investigated milk nutrient composition from three Asian elephant cows over the first 3 years of lactation, including two consecutive lactations in one cow. Body mass gain is presented for three calves during the first year. Milk samples (n = 74) were analyzed for dry matter (DM), fat, crude protein (CP), sugar, ash, calcium (Ca), phosphorus (P), and potassium (K); gross energy (GE) was calculated.

The predominance of type I oligosaccharides is a feature specific to human breast milk.

Human milk and colostrum contain ∼12-13 g/L and ∼22-24 g/L of oligosaccharides, respectively. The chemical structures of >100 human milk oligosaccharides (HMO) have been characterized to date. We determined the concentrations of 10 neutral and 9 acidic colostrum HMO collected during the first 3 d of lactation by using reverse phase HPLC after derivatization with 2-aminopyridine or 1-methyl-3-phenyl-5-pyrazolon.

Structural characterization of neutral and acidic oligosaccharides in the milks of strepsirrhine primates: greater galago, aye-aye, Coquerel's sifaka and mongoose lemur.

The structures of milk oligosaccharides were characterized for four strepsirrhine primates to examine the extent to which they resemble milk oligosaccharides in other primates. Neutral and acidic oligosaccharides were isolated from milk of the greater galago (Galagidae: Otolemur crassicaudatus), aye-aye (Daubentoniidae: Daubentonia madagascariensis), Coquerel's sifaka (Indriidae: Propithecus coquereli) and mongoose lemur (Lemuridae: Eulemur mongoz), and their chemical structures were characterized by (1)H-NMR spectroscopy. The oligosaccharide patterns observed among strepsirrhines did not appear to correlate to phylogeny, sociality or pattern of infant care.

Chemical characterization of milk oligosaccharides of the island flying fox (Pteropus hypomelanus) (Chiroptera: Pteropodidae).

Although a considerable amount of information has accumulated about oligosaccharides in the milk and colostrum of representatives of various mammalian orders, nothing is so far known concerning these sugars in the milk of any bat species (order Chiroptera). In this study, we determined that the following oligosaccharides occur in milk of the island flying fox, Pteropus hypomelanus (Chiroptera: Pteropidae): Gal(α1-3)Gal(β1-4)Glc (isoglobotriose), Gal(β1-4)GlcNAc(β1-3)Gal(β1-4)Glc (lacto-N-neotetraose), Gal(β1-4)GlcNAc(β1-3)[Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc (lacto-N-neohexaose) and Neu5Gc(α2-3)Gal(β1-4)Glc (3'-NGc-SL). However, lactose was found to be the dominant saccharide in this milk, as in most eutherian mammals.

Chemical characterization of oligosaccharides in the milk of six species of New and Old World monkeys.

Human and great ape milks contain a diverse array of milk oligosaccharides, but little is known about the milk oligosaccharides of other primates, and how they differ among taxa. Neutral and acidic oligosaccharides were isolated from the milk of three species of Old World or catarrhine monkeys (Cercopithecidae: rhesus macaque (Macaca mulatta), toque macaque (Macaca sinica) and Hamadryas baboon (Papio hamadryas)) and three of New World or platyrrhine monkeys (Cebidae: tufted capuchin (Cebus apella) and Bolivian squirrel monkey (Saimiri boliviensis); Atelidae: mantled howler (Alouatta palliata)). The milks of these species contained 6-8% total sugar, most of which was lactose: the estimated ratio of oligosaccharides to lactose in Old World monkeys (1:4 to 1:6) was greater than in New World monkeys (1:12 to 1:23).

Chemical characterization of milk oligosaccharides of an African lion (Panthera leo) and a clouded leopard (Neofelis nebulosa).

The Carnivora include the superfamilies Canoidea and Feloidea. In species of Canoidea other than the domestic dog, Canis lupus, the milk contains only traces of lactose and much larger concentrations of oligosaccharides. In this study, lactose was found to be the dominant saccharide in the milk or colostrum of two species of Feloidea, namely the African lion (Panthera leo) and the clouded leopard (Neofelis nebulosa).

Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat.

Patterns of offspring development reflect the availability of energy and nutrients, limitations on an individual's capacity to use available resources, and tradeoffs between the use of nutrients to support current metabolic demands and tissue growth. To determine if the long period of offspring dependency in bats is associated with the need for an advanced state of tissue maturation prior to flight, we examined body composition during postnatal growth in the big brown bat, Eptesicus fuscus. Despite their large size at birth (22% of maternal mass), newborn bats are relatively immature, containing 82% body water in fat-free mass.

Variation in delta13C and delta15N diet-vibrissae trophic discrimination factors in a wild population of California sea otters.

The ability to quantify dietary inputs using stable isotope data depends on accurate estimates of isotopic differences between a consumer (c) and its diet (d), commonly referred to as trophic discrimination factors (TDFs) and denoted by delta(c-d). At present, TDFs are available for only a few mammals and are usually derived in captive settings. The magnitude of TDFs and the degree to which they vary in wild populations is unknown.

Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis).

Differences in diet composition among conspecifics (dietary specialization) have been documented across a broad range of taxonomic groups and habitats, and such variation at the individual level is increasingly recognized as an important component of diversity in trophic interactions. Accurate identification of individual dietary specialization, however, requires longitudinal dietary records that are labor-intensive and cost-prohibitive to obtain for many species. Here we explore the use of stable isotopes (delta13C and delta15N) as a promising technique for detecting and quantifying patterns of individual dietary specialization.

Chemical characterization of oligosaccharides in chimpanzee, bonobo, gorilla, orangutan, and siamang milk or colostrum.

Neutral and acidic oligosaccharides were isolated from the milk or colostrum of four great ape species (chimpanzee (Pan troglodytes), bonobo (Pan paniscus), gorilla (Gorilla gorilla), and orangutan (Pongo pygmaeus)) and one lesser ape species (siamang (Symphalangus syndactylus)), and their chemical structures were characterized by (1)H-NMR spectroscopy. Oligosaccharides containing the type II unit (Gal(beta1-4)GlcNAc) were found exclusively (gorilla and siamang) or predominately (chimpanzee, bonobo, and orangutan) over those containing the type I unit (Gal(beta1-3)GlcNAc). In comparison, type I oligosaccharides predominate over type II oligosaccharides in human milk, whereas nonprimate milk almost always contains only type II oligosaccharides.

Chemical characterization of milk oligosaccharides of a spotted hyena (Crocuta crocuta).

The Carnivora include the superfamilies Canoidea and Feloidea. In species of Canoidea other than Canidae, the milk contains only traces of lactose and much larger concentrations of oligosaccharides. In this study, the following oligosaccharides were characterized in the milk of a spotted hyena, which is a species of Feloidea species: Neu5Ac(alpha2-3)Gal(beta1-4)Glc, Gal(alpha1-3)[Fuc(alpha1-2)]Gal(beta1-4)Glc, Gal(alpha1-3)Gal(beta1-4)Glc and Fuc(alpha1-2)Gal(beta1-4)Glc.

Rhesus macaque milk: magnitude, sources, and consequences of individual variation over lactation.

Lactation represents the greatest postnatal energetic expenditure for mammalian mothers, and a mother's ability to sustain the costs of lactation is influenced by her physical condition. Mothers in good condition may produce infants who weigh more, grow faster, and are more likely to survive than the infants of mothers in poor condition. These effects may be partially mediated through the quantity and quality of milk that mothers produce during lactation.

Fatty acid composition of wild anthropoid primate milks.

Fatty acids in milk reflect the interplay between species-specific physiological mechanisms and maternal diet. Anthropoid primates (apes, Old and New World monkeys) vary in patterns of growth and development and dietary strategies. Milk fatty acid profiles also are predicted to vary widely.

The composition of milk from free-living common marmosets (Callithrix jacchus) in Brazil.

Common marmosets, one of the smallest anthropoid primates, have a relatively high reproductive rate, capable of producing twins or triplets twice per year. Growth and development of infants is relatively rapid, and lactation is relatively short at less than 3 months. Although mean values for the proximate composition (dry matter, protein, fat and sugar) of captive common marmoset milks fall within anthropoid norms, composition is highly variable among individual samples, with concentrations of milk fat ranging from below 1 to over 10%.