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Review

Lactation in Primates: Understanding the Physiology of Lactation from an Evolutionary Perspective

by
Michelle Pascale Hassler
1,2,*,
Alexandre Fabre
3,4,
Valérie Moulin
5,
Lucie Faccin
5,
Julie Gullstrand
5,6,
Alexia Cermolacce
5 and
Pierre Frémondière
1,2,*
1
School of Midwifery, Faculty of Medical and Paramedical Sciences, Aix Marseille University, 13344 Marseille Cedex 15, France
2
UMR 7268 ADES, Aix Marseille University, EFS, CNRS, 13344 Marseille Cedex 15, France
3
APHM, Timone Enfant, Multidisciplinary Paediatrics Department, 13005 Marseille, France
4
MMG, Aix Marseille University, INSERM, 13385 Marseille Cedex 05, France
5
Station of Primatology of Rousset, CNRS, 13790 Rousset, France
6
UMR 7077 CRPN, Aix Marseille University, CNRS, 13003 Marseille, France
*
Authors to whom correspondence should be addressed.
Humans 2024, 4(4), 298-309; https://doi.org/10.3390/humans4040019
Submission received: 22 July 2024 / Revised: 3 September 2024 / Accepted: 19 September 2024 / Published: 25 September 2024
Versions Notes

Abstract

:
Lactation in humans is complex. Understanding the cultural and biological patterns of human breastfeeding requires a global evolutionary analysis that includes observations of other primates. Human breastfeeding may have several specificities, but some features could be shared with other non-human primates. The purpose of this work is to determine what makes human breastfeeding unique from an evolutionary perspective. We consider behavioral as well as biological variables. Human and non-human primates share behavioral characteristics, such as the need to learn breastfeeding skills, and they display an adaptation of the energy density of the milk according to the type of mothering. However, despite having slow-growing, secondarily altricial offspring and rather diluted milk, modern humans spend less time breastfeeding than the great apes, and consequently have shorter interbirth intervals. Milk composition in macro- and micro-constituents changes during lactation, demonstrating evolutionary and ecological adaptation. Among the great apes, the milk of modern humans contains a higher proportion of fats, an equivalent proportion of carbohydrates and proteins, and a greater variety of oligosaccharides involved in brain and immune system development. The microbiome of modern man is less diverse than those of non-human primates, but the presence of HMOs and immunoglobulin A suggests that human milk is particularly adapted to prevent neonatal infections.

1. Introduction

Interest in human lactation is growing in the medical field [1,2] as well as in anthropological literature [3,4,5,6,7]. This helps to improve our understanding of the complex biological mechanisms behind breastfeeding. However, it is essential to consider human lactation within an evolutionary framework. This evolutionary approach in modern humans is fundamental because the human newborn exhibits specific characteristics in comparison with non-human primates. After birth, the brain of the neonate continues to grow at a similar rate typical to that of a fetus, but in an extra-uterine environment. In this context, postnatal care is essential to ensure a child’s survival and subsequent development. As a result, parental investment is greater in humans than in other primates, and often requires family and societal support [6,7]. In order to support this important brain growth, human breast milk must provide a significant amount of energy (evaluated in kilocalorie or kcal), most of which is transferred, in theory, to the infant in the form of milk fat [3]. But this could represent a challenge for the metabolism of the mother, given the considerable burden due to the important amount of energy transfer from the woman’s body to the neonate. During lactation, the mother has to sustain the infant’s growth without depleting her own reserves. This may represent a trade-off from an evolutionary point of view. Indeed, meeting the energy requirement for sustaining the growth of the young permits to ensure his survival; nonetheless, the milk synthesis necessary for this represents the most physiologically costly component of breeding infants [3].
Modern humans give birth to neurologically immature, secondary altricial newborn [8]. This specific state of human newborn is due to two conflicting evolutionary pressures, i.e., bipedalism and encephalization, according to the obstetric dilemma hypothesis [9]. The acquisition of a permanent bipedal locomotion flattens the upper part of the birth canal (i.e., inlet level) from front to back [10,11], and the process of encephalization is responsible for the enlargement of the brain and therefore of the fetal skull [12]. The main consequence of these two antagonistic processes is the ‘premature’ birth of a highly altricial newborn with reduced motor skills. Recent studies suggest that this ‘premature’ birth was already present in Australopithecines, 3.2–1.8 My ago [13,14]. A secondarily altricial newborn needs to be actively carried for a prolonged period after birth. During this period, the lactation is therefore a critical step for the development of the infant. Blomquist et al., [15] suggest that lactation is the last and most energetically demanding stage of the reproductive cycle for a female mammal. The energy cost is particularly high for species that have relatively large neonates and significant brain development [3,16]. According to the secondary altricial state of the newborn, human milk may exhibit specific features that distinguish it from the milk of other primates.
In contrast, modern humans also share certain characteristics with non-human primates. For example, the proportion of macro-constituents of milk (i.e., proteins, fats, carbohydrates) is within the variability of primates. Indeed, human milk is 3.6% fat, 1.2% protein, and 7.4% lactose [3]. In comparison, the milk of Otolemur crassicaudatus is 8% fat, 4.8% protein and 6.4% lactose, while the diluted milk of Eulemur rubriventer is 0.8% fat, 1.1% protein and 8.9% lactose [3]. Moreover, in comparison with other mammals, the human milk is rather diluted to sustain a prolonged lactation period [3,4].
The study of lactation in non-human primates is complex. For example, it is difficult to collect milk samples with a breast pump; in humans, the process is very simple but in non-human primates, using such a device requires a general anesthesia. As a result, our understanding of milk composition remains incomplete and fragmented. Moreover, most studies are based on captive animals, which may not be representative of the milk composition of wild animals. Therefore, the results cannot be generalized for the entire species investigated. The very large number of non-human primate species makes it difficult to gain an overall view of lactation within this order.
It is therefore necessary to carry out a systematic review of the literature in order to observe the differences and similarities in lactation characteristics among non-human primates, and to analyze if, how, and why modern humans share these characteristics. The aim of this literature review is to gain a better understanding of the trade-off between life history and milk composition in primates, to improve our understanding of the human breastfeeding specificities. We use a biocultural approach, first discussing the behavioral characteristics of humans and non-human primates, then looking at how life-history traits are affected by lactation, and finally we address the composition of milk within different primates to investigate the biological characteristics of lactation.

2. Behavioral Characteristics of Primates during Lactation

2.1. Learning and Cooperative Breeding

Breastfeeding is natural, but often requires learning through observation, followed by imitation of the behavior [17]. This learning process is common and essential in most primates. It is passed on in two ways: inter-generationally, where the mother teaches her offspring, and intra-generationally, where individuals teach other individuals of the same age [18].
The learning phase of breastfeeding is very important in modern humans compared with other primates and could represent a major challenge for sustaining the lactation. Maternal stress due to inexperience can lead to a drop in milk production [19].
Modern humans seem to need more help and support than non-human primates [20]. Breastfeeding education and support in modern humans improve breastfeeding rates [21]. This support (e.g., support for mothers to initiate and maintain breastfeeding, recognize and respond to their infants’ cues for feeding, and manage common difficulties) is fundamental to breastfeeding as defined in the Baby-Friendly Hospital Initiative and is part of the ten steps to successful breastfeeding launched by UNICEF and WHO [22].
Learning behavior and cooperative breeding are characteristics of both marmosets and modern humans, but are much more important and necessary in the latter [6]. In non-human primates, learning appropriate mothering and breastfeeding behaviors can be important in particular circumstances. At the beginning of the 20th century, observations made during the first captive births of chimpanzees [23,24] and mountain gorillas [25] showed that the mothers did not breastfeed their babies. This behavior was due to the fact that these females had never seen other females breastfeed [26]. Cases have been reported in zoos, where a lack of nursing has threatened the survival of the young. In such situations, the demonstration of breastfeeding behavior by a caretaker nursing her baby has ensured the survival of a baby gorilla [27] and a baby orangutan [28].
Learning appropriate breastfeeding and mothering behaviors was later shown to be significantly correlated with observation and support from other mothers in non-human primates [17]. Breastfeeding support can be interpreted from the perspective of the cooperative breeding system. Humans are supposed to be cooperative breeders. In a cooperative breeding system, the parents receive support to care for their infants from other adults in the group (i.e., alloparents). For the alloparents, the cost is negligible, but for the parents, this collaborative support significantly alleviates the burden of the nursing. As a consequence, infants are fed by other adults, and the mother can get pregnant earlier. This strategy is therefore supposed to reduce the interbirth interval [6]. Among primates, humans and marmosets are supposed to be cooperative breeders. Cooperative breeding is an important evolutionary advantage, as it enables the infant to compensate for the absence of its mother and adapt to changing situations, and enables the mother to have close pregnancies [6].

2.2. Parental Investment and Child’s Growth

Among the mammals, the mother–infant dyad could be characterized by a type of mothering: some dyads are very cohesive, others very decoupled. The type of mothering influences the frequency of suckling and therefore the density of the milk, which tends to be “diluted” in cohesive species and “concentrated” in decoupled species. In several prosimian species, the mothers “park” their newborns (i.e., “bush-babies”) in nests of leaves for long periods in order to forage for food. In such a situation, milk is enriched with fat to support long periods without feeding, but the concentration of water is reduced [3,29]. Table 1 shows the different types of mothering, with the milk’s characteristics. There are two main types of milk in primates: “dilute”, with low energy density, and “concentrate”, with high energy density. Dilute milk contains more carbohydrates than fats: it has a higher concentration of sugar and water since the proportion of sugar is positively correlated with the water, and negatively correlated with fat [3]. For example, the milk of the Nomascus concolor is 8% lactose, 0.8% fat, and 0.9% protein [3]. However, concentrate milk contains less carbohydrates than fats and the concentration of water is reduced. For example, the milk of the Galago moholi, a Strepsirrhini “bush-baby” species that lives in South Africa, is 12.6% fat, 7.5% protein, and 4.2% lactose [3].
Dilute milk is mostly represented in cohesive dyads, and is of interest in terms of milk yield (i.e., quantity). Concentrate milk characterizes decoupled dyads, and is of interest in terms of milk energy density (i.e., quality). These patterns are common to all mammals [16,30,31,32] and to all primates [3]. The availability of energy during lactation leads to rapid growth and a higher survival rate for Papio anubis offspring [33]. However, a restricted access to food due to unfavorable environmental conditions and/or low social status reduced the amount of milk and the energy density [33]. It has been observed in captivity and wild Papio anubis that the social status of lactating females affects access to food in favor of dominant females [33].
Among mammals, primates exhibit relatively dilute milk [3]. This is due to their slow life-history traits: the period of postnatal growth is long and the infant’s development would deplete the maternal reserve if the energy density of the milk was too high. However, among great apes, human’s milk has a fairly high energy density due to its high fat and protein content [3,16,34,35]. This particular energy density increases the cost of lactation [3,16]. It has been suggested that in humans, women meet this additional cost of lactation by catabolizing fat stores accumulated during pregnancy, reducing physical activity, increasing energy intake, or efficiency of milk synthesis [32].
At the beginning of the postnatal period, because of the fat reserves accumulated during pregnancy, breast milk is highly available in terms of energy, which optimizes the weight and psychomotor development of the young. Infants fed on greater available milk energy will therefore have optimal weight growth and could be more active and confident [36].
Infant humans and non-human primates are all born quadrupedal and have a highly developed ‘grasping’ reflex that enables them to cling to their mothers. Human infants are helpless, secondarily altricial, and need the adult to feed them as their motor skills do not allow them to explore their environment without help [20]. Among the various positional repertoires in primates, humans practice exclusively bipedalism at around 12 and 18 months old [10,37]. In non-human primates, infants can adopt a prone position for the first 2 months which facilitates breastfeeding. This position is predominant until the young have more mature motor skills enabling them to stand on their mother’s side or back [38]. Carrying the baby and providing care on demand will therefore add to the cost of lactation. Caring for the baby is very costly metabolically for its mother [39]. In wild chimpanzees, the energy stress caused by intense breastfeeding in the first two years of life has been demonstrated by elevated urinary insulin levels in lactating females [40]. To alleviate this stress due to lactation, diversification may represent a solution. It is defined as the introduction of solid foods to complement breast milk, and has an influence on the duration of breastfeeding in modern humans. In chimpanzees, growth of young depends solely on breast milk during the first year of life. Even if young chimpanzees can taste solid foods from the age of 6 months, this will only contribute to their growth at around the age of 1 year, i.e., when maternal milk no longer meets their energy requirements [41]. In modern humans, diversification can begin as early as 4 months, so the growth of the infant is no longer entirely dependent on breast milk, which nevertheless remains the infant’s main food. This early introduction of complementary food may prevent allergenic disorders and iron deficiency [42]. WHO recommends exclusive breastfeeding for 6 months, followed by the introduction of complementary food alongside breastfeeding [43]. At 6 months, infants fed exclusively on breast milk need complementary foods to sustain half of the child’s caloric demand, and 1/3 of the caloric demand after the 12th month of life [42,44].

3. Life-History Traits and Breastfeeding

3.1. The Interbirth Interval

Life history reflects unique strategies among species for ensuring efficient growth, optimal reproduction, and increasing life span. Among the life-history traits, interbirth interval is a crucial variable since a shorter interbirth interval increases the number of offspring, but it reduces the time allocated to breeding the young. Although they provide care on demand, modern humans are the only great apes to have short breastfeeding durations [7], offering the possibility to increase fertility and decrease occurrence of annovulation and amenorrhea. During lactation, the secretion of prolactin, which enables milk to be synthesized, inhibits ovarian cycles, resulting in amenorrhea [45]. The inhibition of ovarian cycles depends on the frequency of feedings and the breastfeeding method (i.e., exclusive or mixed with the introduction of other foods). This inhibition is also induced by an energy balance unfavorable to a new pregnancy [46]. In this context, the unfavorable energy balance can be the result of a restriction to food access [46,47,48].
In baboon olive females, the interval between births is reduced when environmental conditions are favorable, i.e., when food is readily available, and when the female belongs to a dominant group [33]. Favorable environmental conditions help the mother to regain weight and reduce energy stress, which improves the energy balance between energy intake from food and its catabolism [33]. In baboons, resumption of ovulatory menstrual cycles is associated with a drop in maternal fecal glucocorticoid levels [49], which may represent the biological signal of the decrease in energy stress. Shorter post-partum amenorrhea was also observed in older females, who no longer invest in their own growth (and are less constrained by this energy demand) but only in that of their young. Social status also influences the length of the birth interval. The dominant baboon olive females have a higher body mass index, resulting in earlier menstrual cycle resumption and a higher reproductive rate than non-dominant baboon females [33]. However, persistent energy stress results in increased interbirth intervals, even in dominant baboon females [33]. During human evolution, a reduction in stress due to food access may have resulted in an increase in fertility. In this context, the mesolithic–neolithic transition is thought to have increased access to food, reduced energy stress, and increased fertility in those human societies [50].

3.2. The Effect of Multiparity

In mammals in general, milk of multiparous females is associated with higher yield, and their offspring gain more weight than the offspring of primiparous females [3]. This could be due to a higher investment in each infant as females get older or a better performance in targeting the physiological needs of the child in multiparous females [51]. In primates, primiparous females produce milk with higher level of glucocorticoids. This results in a nervous and less confident temperament in rhesus macaque offspring, but the weight gain is higher in these infants [52]. However, diversification is more efficient for the young of multiparous mothers, who are more proactive in preparing food (pre-chewing) [41]. In humans, multiparous women find it easier to breastfeed, are less anxious, and have fewer doubts [53]. Multiparous women are more skilled because they have already experienced maternity, and previous breastfeeding experiences, good or bad, have “trained” the mammary glands to produce milk [54].

3.3. Pre- and Post-Weaning Growth

A distinction should be made between “physiological” and “behavioral” weaning. “Physiological” weaning corresponds to the cessation of breastfeeding with a transfer of milk to meet growth needs (i.e., nutritional feeding). “Behavioral” weaning is the cessation of comfort feeding without milk transfer to meet emotional needs. Nutritional and comfort feeding exist in all primates [41]. In humans, the frequency of suction decreases during the first 6 month. At this stage, the intake is stabilized. This stabilization stage continues until the “physiological” or “behavioral” weaning. Diversification at the stabilization stage may represent a unique feature in human lactation and could be an evolutionary advantage for the human infant because it allows him to supplement his milk diet with solid foods until he acquires psychomotor skills that enable him to feed independently [4]. In modern humans, “physiological” and “behavioral” weaning usually take place between 6 months and 3 years of age, which is early in comparison with primate expectations [7]. Indeed, weaning occurs between 4 and 5 years old in chimpanzees [41,55], 2.8 and 4.6 years old in gorillas and between 6 and 7 years old in orangutans [4,55]. This unique human feature could be interpreted as a cooperative breeding feature. Since humans are supposed to be cooperative breeders (a system which optimizes the reproductive cycle of the human group, see above), the early diversification alleviates the cost of exclusive breastfeeding for the mother [6].
The main problem with diversification is to determine when it starts. Consequently, it is difficult to estimate precisely the time of exclusive breastfeeding in non-human primates. However, the analysis of tooth enamel could be useful to gain insights into exclusive breastfeeding duration [55,56]. By analyzing tooth enamel, in particular calcium and barium levels, it is possible to determine the periods of exclusive breastfeeding and the introduction of solid foods in relation to the primates’ living conditions. The calcium and barium contained in breast milk come from maternal reserves and contribute to the skeletal mineralization as well as the dental enamel formation. Consequently, high calcium and barium values in the tooth enamel of infants are a reflection of whether they are exclusively or mixed breastfed [55,56]. In orangutans, the barium and calcium levels increase continuously up to the age of 1 year old [55]. This period is considered as quasi-exclusive breastfeeding. Such an increase was found in a similar study in the molars of rhesus macaques during the first 3 months of life [56]. These levels decrease at the time of diversification. These inverted U-shapes of the calcium and barium concentrations are also found in wild as well as in captive primates [55].

4. Characteristics of the Macro- and Micro-Constituents of Primate Milk

4.1. Fats

The proportion of macro-constituents in milk has been identified in almost all primates, but their involvement in the growth and brain development of offspring remains unknown [3,30]. Among the great apes, modern humans are characterized by a higher proportion of fat in breast milk, compared with the other macro-constituents [3,33,34]. In terms of micro-constituents, 98% of modern human milk fat is composed of triacylglycerides (TAGs). Most TAGs are represented by three long-chain polyunsaturated fatty acid residues esterified to a glycerol molecule. Colostrum, which is the first milk after birth (from birth to the third day of life), contains high levels of long-chain fatty acids and cholesterol, which are involved in the formation of cell membranes and brain development [57]. However, there is some variability in the composition of the colostrum [58] or in the transition time between colostrum and mature milk [59].
The other lipids are around 0.8% for phospholipids and 0.5% for cholesterol [60]. Therefore, the presence of specific lipids in human milk could be due to the unique development of the brain during early infancy. Docosahexaenoic acid (DHA), an omega-3 long-chain polyunsaturated fatty acid derived from milk TAGs, is involved in the development of brain tissue and the membrane of retinal cells [30,60]. However, a comparative analysis of human milk and 11 species of non-human primates shows that the concentration of DHA depends mainly on the mother’s diet [34]. This suggests that the presence of DHA in human milk is not associated with any particular adaptation resulting from the infant’s cerebral growth but reflects a cultural signal associated with food consumption [34,60].

4.2. Carbohydrates and Oligosaccharides

Carbohydrates are the fuel of the brain and are therefore essential for the cerebral growth of the young in modern humans and non-human primates. The main sugar in milk is lactose, which is composed of one molecule of galactose and one molecule of glucose. Lactose accounts for 85% of the carbohydrates in human milk [1] and is digested by lactase in the digestive tract. Colostrum contains two times less lactose than mature milk. This lower level of lactose stimulates the secretion of glucagon, a hyperglycemic agent, which prevents the neonate from hypoglycemia and enhances neonatal metabolic adaptation [61]. The carbohydrate family is also composed of the oligosaccharides. Human oligosaccharides, or HMOs, are currently extensively studied. Table 2 shows the composition of HMOs in different primates. We have identified more than 300 HMOs in human milk. Of these 300 HMOs, 224 are unique to human milk [62]. These HMOs are divided into 13 families of two types, I and II, according to the composition of their main basic structure. This structure is composed of five sugar molecules: D-glucose (Glc), D-galactose (Gal), N-acetylglucosamine (GlcNAc), l-fucose (Fuc), and sialic acid in the form of N-glycolneuraminic (Neu 5GC) or N-acetylneuraminic (Neu5 Ac) [2,62,63]. Type I oligosaccharides predominantly contain the [Gal(β1–3)GlcNAc] structure; type II predominantly contains the [Gal(β1–4)GlcNAc] structure [48,51]. Type I is predominant in modern humans, while type II is predominant in non-human primates [62,64].
HMOs account for 15% of milk carbohydrates and are the third most important solid constituent of milk after lactose and fats [1]. The concentration of HMOs is 3 to 5 times higher in colostrum (20–25 g/L) than in mature milk (5–15 g/L) [1,58,65,66].
The majority of HMOs are not digestible in the small intestine and are found mostly intact in the colon where they become substrates for the gut microbiota [67]. In fact, only 1% to 5% are absorbed in the small intestine, transferred into the blood, and eliminated in the urine.
HMOs act as prebiotic and are therefore mainly involved in the immune system by promoting the development of the microbiota. The microbiota of modern humans are mainly composed of two major groups of commensals, Bifidobacterium and Bacteroides [63], which colonize the digestive tract of newborns. Some bifidobacteria promote the intestinal implantation of other bifidobacteria, and thus play a role in preventing infections [62,68]. The composition of the microbiota is affected by the mode of delivery, but also the gestational age: compared with vaginal births, children born via cesarean section have a microbiota with increased abundance of Firmicutes and lower abundance of Actinobacteria after the first week of life [69]. HMOs are also involved in brain development thanks to the presence of sialic acid, which promotes the connection between neurons in several brain regions [2]. Some factors such as diet, lifestyle, habitat, ethnic origin, and the expression of the Secretor (Se) and Lewis (Le) genes can change the oligosaccharide profiles [1]. In turn, this change could have a deep impact on health status [1]. Four phenotypic profiles have been identified depending on the presence of the Secrector (Se) FUT2 gene which codes for α1–2-fucosyltransferase (2′-FL) or Lewis (Le) FUT3 which codes for α1–3-fucosyltransferase (3-FL): Se+Le+, Se−Le+, Se+Le−, Se−Le+ [51]. The FUT2 gene promotes the proliferation of bifidobacteria involved in defense against pathogenic intestinal bacteria [62,68].
Among mammals, species with a long gestation, long lactation periods, and diluted milk have similar oligosaccharide profiles: HMOs are more fucosylated in response to infectious pressure [62]. Among primates, modern human milk contains a greater variety of oligosaccharides (200) than gorilla milk (50) and chimpanzee milk (130) [70]. But the oligosaccharide profiles of modern humans and chimpanzees show similarities in the proportion of fucosylation and the proportion of oligosaccharide/lactose [62]. Moreover, the variation during lactation of 2′-FL encoded by the FUT2 secretor gene and 3-FL encoded by the FUT3 Lewis gene are nearly identical between chimpanzees and humans [64].

4.3. Proteins

Proteins are the fourth most important solid constituent of milk [1,66]. The protein concentration decreases during the first trimester after birth (22 g/L at birth, 11 g/L around 10–12 weeks of life) [66]. At 6 months, the protein concentration is around 7–8 g/L [71] and this concentration is constant up to 12 months [72]. Several proteins, such as caseins, are involved in the growth of the young, promote digestion of milk, and prevent early infectious diseases. Indeed, bifidogenic k-caseins and immunoglobulins A, G, and M enhance the defense against pathogens [1,66]. The fetus receives maternal antibodies via the placenta during pregnancy (immunoglobulin G) and breastfeeding (immunoglobulin A). The concentration of the immunoglobulin A (Ig As, a major protective factor in human milk) is ten times greater in colostrum than in mature milk. This high concentration of Ig As protects the newborn against respiratory and intestinal infections [57,65,73].
Table 3 shows the concentration of Ig As in modern human, gorilla and orangutan milk. Modern humans have a higher concentration of Ig A than non-human primates throughout lactation. This higher concentration of Ig A could be an immunological adaptation during the mesolithic–neolithic transition. Thus, during this transition human societies were exposed to pathogens due to cohabitation with domestic animals. The concentration of Ig As in the milk of modern humans is 20 to 30 times higher than that of gorillas and orangutans and may reflect an adaptative responses to prevent early zoonoses in newborns [33,65].
Other proteins and cells in breast milk, such as leukocytes and pro- or anti-inflammatory cytokines, help to defend against pathogenic bacteria [59] while lactoferrin chelates the iron essential for bacteria in synergy with lysosymes. In this context, human milk is low in iron to prevent bacterial infection. This may represent an evolutionary advantage to prevent early infections [57].

4.4. The Milk Microbiome

Even if human milk is designed to prevent infectious diseases, milk is not sterile. The milk microbiome is composed of micro-organisms (bacteria, viruses, fungi, parasites) that colonize milk and then the digestive tract of the newborn via the mother’s skin [74].
The milk microbiome (i.e., the microbial diversity in the milk) varies qualitatively and quantitatively depending on the species [75,76], the habitat, the mother’s diet, and the duration of lactation [77]. Comparison between humans and seven species of non-human primates showed that the bacterial strains were 80% similar among the primates. However, these strains could differ quantitatively between species: rhesus macaques have a higher number of bacteria strains than chimpanzees, gorillas, howler monkeys, and modern humans. Cyanobacteria are absent only in human and gorilla milk. Humans appears to have less diversity in the milk microbiome in comparison with other primates. This is probably due to the sedentary lifestyle and hygiene practices in our modern societies.

5. Conclusions

The aim of this work was to gain a better understanding of human lactation from an evolutionary perspective. There are certain limitations to this work: for example, increasingly more studies are focusing on the isotopic analysis of fossil hominin teeth [56,78]. Taking these studies into account would allow a better understanding of how fossil groups, such as Australopithecines, breastfed their young and the energy constraints this represented [78]. We have not taken into account the broader perspective of lactation in mammals in general [75]. This approach would provide a broader view of lactation in lactating species. Breastfeeding is a biological phenomenon that has a cultural component, involving learning in particular that is important for the mother–infant dyad. This variable is a life-history trait for which duration is precisely adjusted to a species’ ecological imperative: associated with interbirth interval, a shorter breastfeeding period increases the number of offspring, but it reduces the time allocated to breeding the young. Some aspects of human breastfeeding alleviate the cost of lactation. Among them, early diversification implies an anticipated independence from the mother’s milk. The human milk composition shows a specific proportion of fatty acids, which could be related to the early brain development of the infant. However, some fatty acids’ proportion (e.g., DHA) are associated with food availability, and do not represent a specific adaptation to human brain growth. The composition of milk micro-constituents, in particular the presence of HMOs and immunoglobulin A, suggest that human milk is particularly designed to prevent early infectious diseases. In human history, the recent mesolithic–neolithic transition may have increased the risk of early infection by exposing newborns to close contact with domestic animals. A possible adaptative response could be the specific composition of the milk. The diversity of the milk microbiome could also be due to our evolutionary history but since modern humans live in a more hygienic environment than non-human primates, their microbiome exhibits less diversity.

Author Contributions

Conceptualization, M.P.H. and P.F.; methodology, M.P.H. and P.F.; validation, A.F., V.M., J.G. and A.C.; writing—original draft preparation, M.P.H. and P.F.; writing—review and editing, A.F., L.F., V.M., J.G. and A.C.; supervision, P.F. and A.F.; funding acquisition, A.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Groupe Francophone d’Hépatologie—Gastroentérologie et Nutrition Pédiatrique and the Biostime Institute Nutrition & Care (BINC).

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Specificities of the milk composition according to the type of mothering [3,29].
Table 1. Specificities of the milk composition according to the type of mothering [3,29].
Type of MotheringEnergy Density of MilkProportion of Macro-ConstituentsInfant’s GrowthSpecies of the Old World
CohesiveDiluteCarbohydrates > FatsSlowCercopithecoides (baboons)
Great apes (modern humans, chimpanzees, gorillas, orangutans
DecoupledConcentrateFats > CarbohydratesFastProsimian
Table 2. The different HMOs’ composition in primate milk 1.
Table 2. The different HMOs’ composition in primate milk 1.
Old World MonkeysRatio of Type I/II Core StructureType of Linked Fucose UnitsN-Glycolneuraminic Acid Neu 5GCOligosacharrides/Lactose Ratio
BonoboII > I2′-FL
3-FL		present1/4 to 1/5
ChimpanzeeII > I present1/4 to 1/5
GorillaII > I2′-FLpresent
OrangutanII > I present1 to 0.8
Modern humanI > II2′-FL
3′-FL		absent1/3 to 1/12
Hamadryas baboonII > I3-FLabsent
Rhesus macaqueII > I3-FLpresent
1 Based on data from [62]; 2′-FL: 2′-fucosyllactose; 3-FL: 3-fucosyllactose; II > I: Predominant type II core structure; I > II: Predominant type I core structure.
Table 3. Comparative table of the concentration of Ig A (in mg/L) in modern human milk and gorilla and orangutan milk [35].
Table 3. Comparative table of the concentration of Ig A (in mg/L) in modern human milk and gorilla and orangutan milk [35].
PrimatesColostrumMature Milk
Modern man600–750120–130
Gorilla67.9-
Orangutan-29.5
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Hassler, M.P.; Fabre, A.; Moulin, V.; Faccin, L.; Gullstrand, J.; Cermolacce, A.; Frémondière, P. Lactation in Primates: Understanding the Physiology of Lactation from an Evolutionary Perspective. Humans 2024, 4, 298-309. https://doi.org/10.3390/humans4040019

AMA Style

Hassler MP, Fabre A, Moulin V, Faccin L, Gullstrand J, Cermolacce A, Frémondière P. Lactation in Primates: Understanding the Physiology of Lactation from an Evolutionary Perspective. Humans. 2024; 4(4):298-309. https://doi.org/10.3390/humans4040019

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Hassler, Michelle Pascale, Alexandre Fabre, Valérie Moulin, Lucie Faccin, Julie Gullstrand, Alexia Cermolacce, and Pierre Frémondière. 2024. "Lactation in Primates: Understanding the Physiology of Lactation from an Evolutionary Perspective" Humans 4, no. 4: 298-309. https://doi.org/10.3390/humans4040019

APA Style

Hassler, M. P., Fabre, A., Moulin, V., Faccin, L., Gullstrand, J., Cermolacce, A., & Frémondière, P. (2024). Lactation in Primates: Understanding the Physiology of Lactation from an Evolutionary Perspective. Humans, 4(4), 298-309. https://doi.org/10.3390/humans4040019

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