Duration of Breast Feeding in Ancestral Environments
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Contemporary studies reveal widespread global variation in breastfeeding patterns, providing a fascinating example of human behavioral flexibility (Sellen 2009). However, human infant behavior and physiology evolved under environmental conditions that differ notably from those in which most humans live today. Current evidence places the origin of Homo sapiens at ~200,000 years ago (Conroy and Pontzer 2012). Ancestral Homo sapiens were hunter-gatherers for most of the species’ existence until agriculture, urbanization, and industrialization emerged-all within the past ~11,000 years (Ellis et al. 2013). Under ancestral conditions of hunting, gathering, and high infant mortality, infant survival depended on the immunological, hormonal, and nutritional factors in maternal breastmilk (Hinde and Milligan 2011; Volk 2009).
Prolonged breastfeeding is the norm in most contemporary hunter-gatherer populations, and biological patterns of infant digestive and masticatory development similarly suggest that this pattern is also the human ancestral norm (Sellen 2009). Mean age of introduction of solid foods and total breastfeeding durations were 5.0 ± 4.0 months and 29.0 ± 10.0 months, respectively, in an analysis of 113 nonindustrialized populations; cultural groups with “extractive” (hunter-gatherer) economies had longer overall breastfeeding durations than pastoralists and agriculturalists (Sellen and Smay 2001). In stark contrast, breastfeeding rates are low and durations short in many contemporary, industrialized settings, perhaps because technology and medicine minimize selective pressures that have shaped infant biology throughout human evolutionary history (Ball 2008; McKenna and McDade 2005). Life history theory, a branch of evolutionary ecology, provides a useful framework for analyzing population differences in breastfeeding durations, and for inferring breastfeeding patterns throughout human evolutionary history.
Life history theory (LHT) posits that the behavior and life schedules of organisms are shaped by natural selection to maximize biological “fitness” or reproductive success – usually defined by proxy as “the surviving number of offspring of an individual” (Wilson 1975). Biological fitness maximization occurs when energetic resources are optimally allocated to competing life history functions (brain and body growth, survival/maintenance, and reproduction) (Smith and Fretwell 1974; Charnov and Berrigan 1993; Charnov 2004). Organisms have fixed energy budgets, so energetic “trade-offs” occur between competing life history functions (e.g., upregulated survival effort diminishes growth effort) (Stearns 1989) and are most pronounced under conditions of resource scarcity (Tschirren and Richner 2006).
According to LHT, many parenting behaviors are shaped by natural selection. Parental investment is defined as “resource allocation to one offspring that diminishes a parent’s ability to invest in another” (Trivers 1972). In mammalian mating systems, females bear the energetic burdens of gestation and lactation; in most human societies, mothers are higher investing than fathers and provide the majority of offspring care (Konner 2005). Lactation represents a particularly energetically costly form of maternal investment, and as such it “trades off” with other maternal life history functions (e.g., time and energy for self-maintenance, production of food resources, care of other existing offspring, and production of additional offspring) (Prentice et al. 1996). Weaning (the gradual cessation of breastfeeding) can therefore become a source of conflict between mothers and infants (Trivers 1974).
Weaning conflict exists due to asymmetry in genetic relatedness between mothers and offspring (Trivers 1974). Mothers are entirely related to themselves, and equally related (by ~50%) to each of their different offspring. Infants are entirely related to themselves, but share fewer common genes with their mothers, and any existing or future (nonidentical twin) siblings. Mothers must therefore partition investment optimally between multiple (current and future) offspring, and between self-maintenance and reproductive effort, to efficiently maximize individual lifetime reproductive success (Lee 1996). However, in accordance with Hamilton’s rule, offspring should prioritize their individual fitness over that of their kin; weanlings may adopt behavioral tactics to continue to extract maternal resources (e.g., breastmilk) (Hamilton 1964; Trivers 1974). Common behaviors include smiling, nuzzling, begging, crying, and tantrums, with weanlings sometimes demanding more than mothers are willing to provide (Haig 2014; Trivers 1974). Continued suckling is associated with maternal lactational amenorrhea (postpartum anovulation), which improves weanling fitness by delaying conception and birth of a younger sibling (Haig 2014). Compelling new research suggests that maternal physiology may, in turn, be evolved to modify offspring behavior; for example, “bioactive components in maternal milk may be influencing the infant microbiota to shift the infant phenotype toward the mother’s optima for investment” (Allen-Blevins et al. 2015, p. 117).
Phylogenetic Context of Human Infancy
Life history theory is also used to make phylogenetic comparisons across animal taxa (Charnov and Berrigan 1993; Lee 1996). Several distinguishing human life history traits (slow fetal growth, infant altriciality, short infancy durations, prolonged juvenility, and high fertility) likely evolved in the past ~2 million years, in conjunction with rapid increases in human brain size (Bogin 1998). The human fetus grows somewhat slowly in utero compared to fetal growth in other ape species; humans are born with ~30% of their adult brain size (compared to ~40% for chimpanzees), and human newborns are neurologically altricial compared to other newborn primates (DeSilva and Lesnik 2006). Human infancy – defined here as the period of maternal lactational provisioning – is also fairly short (~1–3 years) in comparison to other great apes (~3–8 years) (Kennedy 2005; Lee 1996). In contrast, human childhood and juvenility are prolonged in comparison to other apes (Bogin 1998).
In nonhuman primates, the end of infancy is marked by the eruption of first permanent molars; in humans, weaning occurs roughly 3–5 years the first permanent molars erupt (Smith and Tompkins 1995). In concordance with a broader pattern characteristic of mammalian species where mothers birth altricial, singleton infants, human weaning tends to be a protracted process in most nonindustrialized populations (Whitehead 1995; Sellen 2009). Notably, in most human societies, nonmaternal group members (fathers, grandparents, siblings, extended kin) assist with provisioning of recently weaned children (Kramer 2010). This practice accelerates the resumption of maternal ovulation post birth, shortens human interbirth intervals relative to other great apes, and facilitates high fertility rates that have come to characterize the human life course (Humphrey 2010).
Breastfeeding and the Weaning Process
Exclusive breastfeeding: The period in which infant nutritional and immunological needs are met exclusively through consumption of mother’s milk. The relative benefits of breastfeeding decline as infants approach 6 months of age, because maternal milk output is limited and infant energetic requirements increase continuously (McDade and Worthman 1998). Although exclusive breastfeeding is not practiced in some settings (in lieu of formula and other breastmilk substitutes), it is essential to infant survival in most past and present socio-ecological contexts.
Partial breastfeeding: This stage is marked by the introduction of liquid and solid weaning foods that are regularly consumed by infants in conjunction with breast milk. Because increased gastrointestinal infection is associated with the introduction of infant foods, they may be specially prepared to facilitate digestion and minimize antigen exposure (Fouts et al. 2005). Throughout this protracted weaning process, nonmaternal group members often support young children through nutritional provisioning of processed weaning foods (Humphrey 2010). Partial feeding may last until a child is two or older in nonindustrialized populations (Sellen and Smay 2001). In contrast, initial infant food provisioning is often synonymous with cessation of breastfeeding in some very modernized contexts (Whitehead 1995).
Nutritional independence: In most mammals, by the onset of nutritional independence (end of the weaning transition) offspring have attained sufficient physical maturity and competence to undertake independent traveling, foraging, food processing, and digestion (Lee 1996). Because human weanlings are not capable of successful independent foraging, they continue to receive foods provisioned by mothers, other kin, and unrelated alloparents (Bogin 1998; Kramer 2010). Provisioned post-weaning foods tend to be energy dense, and provide nutrients required to fuel children’s brain growth, which continues up to 7 years of age and beyond (Kennedy 2005).
Threshold Model of Weaning
Phylogenetic life history comparisons reveal positive correlations between adult and neonatal body weight, adult and neonate brain weight, and interbirth intervals (a proxy for weaning age) (Harvey and Clutton-Brock 1985; Lee 1996). In large-bodied mammals, offspring are typically weaned by a maximum “threshold” body size, which is achieved when the infant grows to roughly quadruple their birth weight (Lee 1996). According to this model, a human neonate born at 3.3 kg will be weaned at 13.2 kg (10.6–16.2), which “corresponds to an age of 2.5 years (1.3–3.9) for breastfed male babies on the 50th growth centile” (Humphrey 2010). Weaning is often thought to occur at this threshold because infant energetic requirements come to exceed the upper limits of maternal metabolic capacity (Lee 1996). It has also been suggested that slow infant growth leads to longer breastfeeding durations in nutritionally and epidemiologically risky environments (Hochberg 2011). In general, infant growth rates are rapid in the early postnatal phase, decelerate across infancy, and then abruptly accelerate at the onset of the biologically salient transition into childhood. In hunter-gatherer populations, this transition occurs near the mean weaning age (2–3 years) whereas in affluent Westernized countries, it occurs at ~6–12 months (Hochberg 2011).
Facultative Model of Weaning
The “shifting weaning optima” model states that weaning age is facultative and occurs when the maternal costs of prolonged lactation outweigh the infant benefits (Sellen and Smay 2001). A conceptually similar “evolutionary trade-offs” model was proposed by Tully and Ball (2013), more explicitly incorporating Trivers’ (1974) model of parent–offspring conflict. According to these models, prolonged breastfeeding will persist in settings where its benefits to infants are high (e.g., environments of high infectious disease morbidity) and/or when actual and/or perceived maternal time, energy, social, and opportunity costs are low (McDade and Worthman 1998; Tully and Ball 2013; Veile and Kramer 2017). Support for a “shifting weaning optima” has been at least partly supported through qualitative assessments of costs and benefits of breastfeeding in different environments (Veile and Kramer 2017), though it should be noted that the costs and benefits of breastfeeding are challenging to operationalize.
The duration of breastfeeding in human ancestral environments can be inferred through investigations of ancient human fossil remains, extant and extinct nonhuman primates, and contemporary hunter-gatherer populations. Human breastfeeding durations are simultaneously shaped by divergent mother–infant fitness interests, local ecologies, and cultural norms. Despite substantial intraspecific variability in breastfeeding patterns, combined bodies of evidence suggest that breastfeeding for 2 or more years is the human ancestral norm (Sellen 2009). Though the biological fitness costs of not breastfeeding are reduced in many contemporary modernized settings, prolonged breastfeeding is still an economical, nutritional, and hygienic strategy for maximizing infant survival in many parts of the world.
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