Chapter 22
The Evolutionary Ecology of the Family

Ruth Mace

Introduction

Humans live in families. A central relationship in virtually all human social systems is that between husband and wife, although there are relatively few systems where a pair-bonded couple live entirely independently (Harrell, 1997). Hunter-gatherers mostly had (serially) monogamous marriage, no heritable wealth of consequence, and relatively egalitarian social systems. Hunter-gatherer bands were relatively fluid associations of groups of nuclear families that could be based on matrilateral or patrilateral or mixed kinship, friendship, or convenience (Apicella, Marlowe, Fowler, & Christakis, 2012; K. R. Hill et al., 2011; Marlowe, 2005). Changes in subsistence strategy were instrumental in many of the major evolutionary transitions in human evolution, including in the family; particularly important was the advent of agriculture. Access to heritable resources, that greatly influences the future reproductive success of descendants, generates inequalities in wealth and political power (Kaplan, Hooper, & Gurven, 2009). Fertility increased and population densities increased with the advent of agriculture; more complex political systems emerged, correlating with ethnolinguistic groups becoming larger (Currie & Mace, 2009; Johnson & Earle, 2000). Patterns of marriage, residence, descent, and inheritance became both more formalized and probably more diverse and with much more sex-biased dispersal. Thus, understanding human families involves understanding their biological and cultural evolution. The framework of evolutionary ecology has been used to investigate both these aspects and their coevolution.

The Coevolution of Human Life History with Social Organization

Given that humans have lived as hunter-gatherers for most of their evolutionary histories, a large part of our physiology and psychology, including our key life-history traits such as age of onset and termination of fecundity and senescence, presumably arose as adaptations to this form of subsistence. Human female life histories have features that are rather different from that of other apes, including long childhoods, rapid reproductive rate after puberty, and then female menopause followed by a long postreproductive life. Explanations for these patterns are varied, but most are related to the cooperative and competitive relationships in families (Hawkes, O'Connell, Blurton Jones, Alvarez, & Charnov, 1998; K. Hill, 1993; Mace, 2000). The combination of relatively short interbirth intervals and long childhood means that families include several dependent children at the same time, and that is costly for mothers. The phenomenon of mothers raising children alone is not observed as normative in any traditional human social system; human mothers nearly always rely on help from their husband to a greater or lesser extent, and often also on the extended family, including grandmothers.

Menopause might be selected for because grandmothers were cooperative breeders and grandmothers were helping their daughters reproduce (Hawkes et al., 1998). This hypothesis stimulated a great increase in interest in kin effects on human fertility, providing an example of how evolutionary theories have helped to set the agenda beyond the evolutionary field in areas such as demography. Speculation on menopause goes back to Williams (1957) and (Hamilton, 1966). A more formal “grandmother hypothesis” that human menopause might be selected for by kin selection favoring older mothers investing in their grandchildren rather than continuing to reproduce themselves was developed (Hawkes et al., 1998). There is now considerable evidence that grandmothers enhance the reproductive success of their offspring (reviewed in (Sear & Mace, 2008). Maternal grandmothers benefit grandchild survival across a wide range of societies. Paternal grandmothers may also be of help, especially in hunter-gatherers (Crittenden & Marlowe, 2008), but their effects are more mixed.

Not all researchers agree about whether the grandmother effect, on its own, is enough for menopause to be favored by natural selection. Some favor the view that the effect of mothers on offspring is more important (Pavard, Koons, & Heyer, 2007; Peccei, 2001), often described as the “mother hypothesis.” The mother and grandmother hypotheses are adaptive models that are fairly similar in that they both require some benefit for a separation of reproductive aging from somatic aging. In contrast, some contend that menopause is just due to physiological constraints, such as the temporal viability of female ova (K. Hill & Hurtado, 1991). Postreproductive life could then have evolved as the derived trait, with fertility constrained to halt at 50 (Hawkes et al., 1998; Kim, Coxworth, & Hawkes, 2012). Mathematical models informed by data have had mixed results: They either fail to predict any fitness benefit associated with terminating reproduction so long before death (Hill & Hurtado, 1996) or find that benefits of combined mother and grandmother effects on fertility and age-related increases in maternal mortality may be enough to favor menopause (Pavard & Branger, 2012; Shanley, Sear, Mace, & Kirkwood, 2007), but effects are possibly rather marginal.

Implicit in most of the various models of the grandmother hypothesis is the notion that mothers and daughters are in reproductive competition, because it is assumed only nonreproductive grandmothers can really help her daughter's reproduction. It is striking how little human female generations overlap (Figure 22.1); as a daughter reaches reproductive age, her mother reaches menopause, and as she reaches menopause, her mother dies. However, although reproductive conflict predicts that reproductive generations should reduce overlap, it does not address why it is the older woman that is foregoing reproduction rather than the younger one, as is generally the case in most cooperatively breeding birds or mammals (Clutton-Brock, Hodge, Flower, Spong, & Young, 2010; Hatchwell & Komdeur, 2000). The competition between mothers and grandmothers is particularly intense in species in which females disperse, as female dispersal means that older females are not closely related to younger breeding females in their group (Cant & Johnstone, 2008; Johnstone & Cant, 2010). Female dispersal is unusual among mammals, but is the most common condition in chimpanzees (Pan troglodytes) and we assume was the case in ancestral humans, although there is variation in residence patterns of contemporary hunter-gatherers (K. R. Hill et al., 2011). Under patrilocal residence (when females disperse at breeding age and males do not disperse), adult female relatedness to the group will be low at the point of arrival in a new group, and the other females in the group will normally be only distantly related if at all. A female's relatedness to the co-resident group will gradually increase with age as her offspring (particularly sons who do not disperse) are born and then grow up to reproduce themselves. We have shown that this pattern of relatedness does apply in the case of patrilocal compounds (where fathers, sons, and brothers and their families co-reside) in rural Gambia (Mace & Alvergne, 2012). When older women find themselves in competition with their sons' spouse for reproductive resources, there is an essential asymmetry in that the older woman is related to her son's offspring (and thus will suffer a fitness cost in harming her son's wife's reproduction), whereas the son's wife has no relatedness to the older women's offspring, so natural selection does not favor helping her husband's mother reproduce. Evolutionarily stable strategy (ESS) models show that the younger woman is more likely to win the competition, and the older women is destined to become the sterile helper (Cant & Johnstone, 2008). They draw on earlier models that show how reproductive conflict in communally breeding species generally means that, although dominant breeders use more of the resources needed for reproduction than do less dominant ones, it may well be in the genetic interest of less dominant individuals to help more powerful kin reproduce rather than pay the costs of trying to compete with them to reproduce (Reeve, Emlen, & Keller, 1998). Johnstone and Cant (2010) argue that increasing relatedness to the group with age helps explain late life low fertility in whales and primates in which females either disperse or mate outside the group; humans usually fall into the former category. Thus menopause could be linked to sex-biased dispersal patterns. This is interesting, because some had assumed that previous grandmother hypotheses would require matrilocal societies, because maternal grandmothers appear to be the most helpful. This conflict under female-biased dispersal hypothesis suggests the opposite. This theory for menopause only holds if female–female conflict is the main determinant of reproductive schedules. Fathers and sons co-reside in patrilocal societies, and fathers will typically win in conflict with sons, so if males determine the outcome of reproductive conflict, then female dispersal would not predict menopause (Ji, Xu, & Mace, 2014). Dominance and polygyny, not just dispersal, matter in determining patterns of reproduction. Models of genomic conflict between maternally and paternally inherited genes suggest conflict under many circumstances, and predict that fertility could be surpressed by a number of factors, not just sex-biased dispersal (Úbeda, Ohtsuki, & Gardner, 2014). So the evolutionary basis of menopause is still an area of ongoing research.

Figure 22.1 Age at Time of Birth for Mothers, Maternal Grandmothers, and Paternal Grandmothers in Rural Gambia. Source: From Mace and Alvergne, 2012.

When wealth from parents or their kin is needed for marriage, parents can control their son's reproductive opportunities, and by delaying their son's marriage, can reduce intergenerational reproductive conflict. In rural Gambian Mandinka (who are farmers), the cultural norm of late male marriage reduces overlap in the reproductive span of mothers and daughter's-in-law almost to zero (Figure 22.1; Mace & Alvergne, 2012). In the very few cases of a daughter-in-law's reproduction overlapping with their mother-in-law's reproduction, the costs seem to be high (Lahdenpera, Gillespie, Lummaa, & Russell, 2012). When daughters move out of the natal household at marriage or shortly after first birth, intergenerational competition between female kin for household resources is presumably reduced by patrilocality (also known as virilocality). Thus fertility patterns could be coevolving with human kinship systems, with earlier female age at first birth and possibly later male age at first birth associated with patrilocal residence (Marlowe & Berbesque, 2012). Kinship, residence, and marriage norms in human societies can themselves be seen as cultural adaptations to reduce reproductive conflict in families (Mace, 2013).

The Coevolution of Kinship, Marriage, and Subsistence Systems

The cultural norms of marriage, kinship, and descent are in large part products of the socioeconomic system on which societies are based. Hence human behavioral ecology is fundamental to understanding this foundational area of anthropology.

Polygyny, Monogamy, and Polyandry

As is well known to behavioural ecologists, if males are able to monopolize access to territory that has the resources required for breeding, then that resource can be used to attract females, who will mate polygynously if need be, to acquire that resource. Such resource-defense polygyny, not dissimilar to that described in birds (Orians, 1969), is also common in humans that have heritable wealth or a resource that can be monopolized (Borgerhoff Mulder, 1990). As in other species, such polygynous systems can only really emerge when there are sufficient resources for females to raise their children without a great deal of individual help from fathers. Resources such as livestock are particularly associated with polygynous marriage and male-biased wealth inheritance (Hartung, 1982). Men compete for resources and use those resources to compete for marriage partners. They compete with their own brothers if families are the main source of resources. Polygynous societies contain plenty of unmarried men. Under polygyny, because females are in demand, the parents of daughters can exploit this to demand bride price (a wealth transfer from the groom to the bride's family). Pastoralist systems typically show all these characteristics, because livestock are walking money and not as hard work as extensive crop farming systems for example. Gabbra pastoralists, who herd camels in northern Kenya, can enhance their number of grandchildren more by passing on livestock to their sons (enabling them to marry earlier and more often) than by giving camels to daughters (Mace, 1996); so under resource-based polygyny, patrilineal (male-biased) wealth inheritance norms will maximize the inclusive fitness of the parents.

Monogamy (and occasional polyandry) in hunter-gatherers may relate to resource constraints and difficulty of a male supporting more than one female; one such case is the Inuit of the high Arctic. This is known as ecologically imposed monogamy (Alexander, Hoogland, Howard, Noonan, & Sherman, 1979). But monogamy is also widespread in wealthy societies, especially in Eurasia, including in populations that do not appear to be especially poor, suggesting the need for other explanations. In birds, monogamy is thought to be due to the need for male provisioning, and in primates it is more likely to be related to the avoidance of infanticide (Opie, Atkinson, Dunbar, & Shultz, 2013). Both issues are important in human social evolution. Parental investment, including inherited wealth, is probably key to the cultural evolution of monogamy in agricultural societies. In polygynous societies, the advantages to women of marrying a wealthy male are diluted by the fact that wealth will have to be shared with future co-wives and their offspring; thus male competition for females is much more intense than female competition for males. Yet in monogamous societies, the wife's offspring enjoy sole rights to the inheritance; so females should compete to marry the wealthiest males. This competition generates dowry, that is the payment of money from the bride's family to the groom's family, to make their daughters more attractive enhancing their marriage prospects (Gaulin & Boster, 1990). In parts of India, where dowry is a significant cost to parents required to marry off daughters, females with several older sisters are even at risk of infanticide (Dickemann, 1979). The benefits to males of monogamous marriage are more difficult to explain. Modelling shows that an ESS can emerge if females reward exclusive male investment with their sexual fidelity, but only in ecosystems where the returns on male investment are high with diminishing returns when resources are partitioned (Fortunato & Archetti, 2010). Monogamous marriage is seen where intensive agriculture led to scarcity of land, with depletion in the value of estates through partitioning among multiple heirs.

But the role of infanticide in the evolution of human monogamy cannot be overlooked. It was probably common among hunter-gatherers, in part as a means of controlling fertility rate, when mothers or fathers felt unable to support further offspring. The idea that parental investment is linked to mating strategies, mortality risks, and all other life-history traits was not well understood prior to evolutionary analyses of demographic data. Parental investment cannot be taken as a given and reduced paternal investment is one of the costs of mothers mating with multiple males. The death of the father is a significant cause of infanticide in the Ache (K. Hill & Hurtado, 1996), as other families are not willing to help support orphans or children without fathers. Infanticide of the sort seen in several mammals, such as in langurs (Hrdy, 1990), gorillas, or lions, where incoming males systematically kill infants to induce females to return to oestrus, is not what happens in humans. Nonetheless, one of the most important findings on human parenting was the key work on child abuse and child homicide, which highlighted the role of unrelated partners of mothers in the abuse and neglect or homicide of children from previous relationships (Daly & Wilson, 1988). Since this early study, the results have been replicated in different settings all over the world, with the notable exception of Sweden (Temrin, Nordlund, Rying, & Tullberg, 2011). These findings have clear public-policy implications, not that they have always been given the attention by policy-makers that they deserve (Daly & Perry, 2011). Infanticide is clearly an extreme situation, but the insight that unrelated father-figures are likely to be more of a cause of stress or conflict than genetic fathers applies even in cases where no abuse is involved. In a study of accidental deaths in Australia (ranging from traffic accidents to falling into swimming pools, when no foul play is involved), genetic parents, be they one single parent or two married parents, were less likely to lose their child to such an accident than if young children were living with one genetic parent and one nongenetic parent (Tooley, Karakis, Stokes, & Ozanne-Smith, 2006). In a cohort of normal UK children aged 10, father absence is associated with a tiny reduction in stature over father-present families, and a bit larger reduction in stature is correlated with an unrelated co-resident father figure (Figure 22.2; results from Lawson & Mace, 2009). Some of the costs of a new partnership may be due to the mother diverting her attention toward the new partner, and any new offspring fathered by him, as much as maltreatment being attributable to actions by the new partner himself. There could be additional costs of father absence to older children in terms of monetary investments and wealth inheritance, and hence on marriage prospects, as has been shown in a study of paternal death in India (Shenk & Scelza, 2012). All these effects are relevant to the evolutionary basis of monogamous marriage, and the potential fitness costs to fathers of divorce, as fathers have to trade off the fitness costs of leaving one family against the benefits of starting another.

Figure 22.2 Height Difference in mm in Children Aged 10 With Either Father Absent (black bars) or Stepfather Present (gray bars), Relative to Height of 10-Year-Olds Who Live With Both Genetic Parents, for (a) Boys and (b) Girls. Source: Data from Lawson and Mace, 2009.

Only a tiny proportion of human cultures worldwide show polyandrous marriage (Murdock, 1967), which is normally fraternal (two or more brothers marry one wife), no doubt due to the risks of a mother's unrelated sexual partner co-residing with her children from another father. In the patrilineal Sherpa of the Himalyas, farming habitat is saturated, as it is restricted to a few river valleys, so there are few opportunities to disperse and set up neolocal farms. It appears that competition between brothers can only be resolved by all brothers marrying the same wife—the ultimate in reproductive sharing. Younger brothers do badly, in terms of direct fitness (Haddix, 2001). But sharing some paternity with a dominant elder brother (albeit the smaller part) can be better than fighting with him for the farm or for more access to their shared wife (Ji et al., 2014). When resource constraints were lifted by the emergence of jobs outside farming, then the younger Sherpa brothers quickly left polyandrous marriages to set up nuclear families (Haddix, 2001).

Residence, Descent, and Wealth Inheritance

Most human societies trace their ancestry predominantly through one side of the family or the other. This is usually reflected in their naming system and frequently prioritizes either the patrilineal or matrilineal line over the other in terms of the inheritance of both titles and material wealth. Within lineal descent systems, patriliny is the most common pattern worldwide. This is because of the benefits to males of controlling resources, particularly important after the advent of agriculture and heritable wealth that has been discussed earlier (in section titled Polygyny, Monogamy, and Polyandry). Patrilineal wealth inheritance and patrilocal residence are usually found together for the same reason. Females in patrilineal, patrilocal, social systems are foregoing the benefits of proximity to their female kin for the advantages of access to male-owned resources, such as land and livestock. The price could be severe female–female conflict, as described in the Dogon in Mali who do not seem to be well-described as cooperative breeders (Strassmann, 2011).

A significant minority (about 17%) of systems described in the Ethnographic Atlas (Murdock, 1967) are matrilineal. Marriage bonds are often weak in matrilineal systems, with women frequently having several husbands over the course of their lives; multiple paternity has few implications for heritable resources as wealth and titles are generally passed down the female line. The ecology that is predictive of matriliny is biased toward systems with a lack of resources that can be easily monopolized by males to attract females. In Africa, it is strongly associated with the absence of livestock herding (Aberle, 1961; Holden & Mace, 2003). In other parts of the world, matriliny has been proposed to be associated with high male mortality and/or male absence rates, either because of warfare, as in some matrilineal native American groups (Keegan & Maclachlan, 1989), or with trade networks and ocean fishing as in the Pacific (Hage & Marck, 2003). Whatever the underlying ecology, women in matrilineal systems rely on mothers, daughters, and sisters to support their family, as help from husbands, or any males, is often transitory. Paternity certainty tends to be low in matrilineal systems, although the extent to which this is a cause or consequence of matrilineal descent systems is a matter of debate (Hartung, 1985). Matrilineal systems represent a puzzle to evolutionary (and other) anthropologists, because it is unclear why a male should invest in his sister's offspring rather than that of his wife. Even if paternity uncertainty is at the highest levels observed in human societies (for example as seen in the Himba; (Scelza, 2011), the relatedness to his wife's offspring is higher than to his sister's offspring; this would change only if paternity certainty were less than 0.268 (Greene, 1978), which is unrealistically high. However if sisters are breeding communally, and a male's investment is shared by the communal household, then the fitness payoffs change in favor of matrilineal investment (Wu et al., 2013). Figure 22.3 shows the results of Wu et al.'s model of the optimal allocation of male investment between his wife's household and his sister's household as a function of the number of sisters co-residing in a communal household. In the case of just one breeding female per family, p (paternity certainty) would again have to be less than 0.268 for a male to invest more in the matriline (the same figure Greene predicts); however if two or three sisters co-reside and live communally, then the payoffs quickly change against investing in the wife's household in favor of the sister's household (i.e. the natal household) where all offspring are genetic relatives. The more sisters or female kin breed communally, the more matrilineal investment is favored. Note that the number of communally breeding sisters (n) is a more important determinant of matrilineal investment than is paternity certainty (p) within realistic ranges of p. The Mosuo of southwestern China are one of the most matrilineal societies ever described, as neither sex disperses and brothers and sisters live together throughout life and work on communal farms; household food (mostly grains, pork. and fish) is shared, so males will not gain much fitness by investing in feeding a household full of their wives' sisters offspring (to whom they are unrelated) (Wu et al., 2013). Sexual partnerships in the Mosuo are described as “walking” or “visiting marriages” as males only stay with partners overnight, but return home in the morning; fathers invest little in their offspring. The fact that these traditional unions do not imply exclusivity or co-residence, shows that marriage, as usually understood, is not fundamental to all societies.

Figure 22.3 Optimal Resource Allocation From Males Choosing Between Natal or Spousal Household. The optimal resource allocation of males' effort to either their sister's farm (x*, upper line) or the wife's farm (y*, lower line) as function of paternity certainty (p) and the number of sisters that co-reside in a household (n). Note that for nuclear families (n = 1) only after p < 0.268 does investment in a sister exceed investment in a wife. But when n ≥ 2 in a communal household, matrilineal investment is increasingly favored. Source: From Wu et al. (2013).

Monogamous marriage and neolocal nuclear households are now becoming more common in the Mosuo, in part because it is encouraged by Chinese law and family policy, but also due to economic changes. The emergence of tourism in the Mosuo area has enabled some individuals to raise extra money independent of the farm (through activities such as tourist hotels), making them more likely to leave the communal households and set up neolocal households living as nuclear families (Mattison, 2010). This shows how the communal breeding observed here may be based on constraints on dispersal, as it is believed to be in many communal breeders in the animal kingdom (Hatchwell & Komdeur, 2000). An example of communal breeding by brothers comes from polyandrous Tibetan Sherpa households in the Himalayas (discussed in section titled Polygyny, Monogamy, and Polyandry). Thus, both the matrilineal Mosuo and the polyandrous, patrilineal Tibetans show how communally breeding households can emerge out of constraints on dispersal, and they become unstable when there is a relaxation of these constraints.

Social systems rarely leave any trace in the archaeological record. Sex-specific genetic patterns are often argued to reflect aspects of past human mating systems (Kayser et al., 2003; Seielstad, Minch, & Cavalli-Sforza, 1998), although such inferences are possibly picking up genetic patterns generated after the advent of agriculture and other aspects of population structure (Heyer, Chaix, Pavard, & Austerlitz, 2012; Wilkins & Marlowe, 2006). Most ethnography is confined to the present and recent history relying on living memory or on written or oral histories as sources. Phylogenetic comparative methods provide a powerful set of statistical tools that have been developed by evolutionary biologists for understanding diversity, and these go beyond just seeking correlation to examine a whole host of evolutionary processes and questions, including rates of change, ancestral states, the tempo and mode of evolution, phylogenetic signal, and reticulation (Pagel, 1999). Cultural phylogenetic techniques make use of language phylogenies to do similar analyses across human cultures (Mace & Pagel, 1994) and potentially enable us to put prehistory back into anthropology (Mace, Holden, & Shennan, 2005). These were the methods used to show that in Bantu-speaking populations, patrilineal social systems were associated with pastoralism, whereas matrilineal systems were associated with a lack of cattle-keeping (Holden & Mace, 2003) and the model of direction of change that best fits the data confirmed the hypothesis that a transition to pastoralism precedes a switch to patrilineal descent systems, suggesting causation.

Phylogenetic techniques rely on using the extant distribution of traits, and the phylogeny, to infer which evolutionary processes were most likely to have generated that distribution (Pagel, 1999; Pagel & Meade, 2006). Implicit in the method is the inference of ancestral conditions. We have used these techniques to show that the most likely ancestral condition of Proto-Malayo-Polynesian (∼4,500 years ago) was matrilineal and matrilocal, with patrilocal systems evolving later on in the Austronesian family (Jordan, Gray, Greenhill, & Mace, 2009). Similarly we have been able to show that dowry and monogamy were probably ancestral in Indo-Europeans (Fortunato, Holden, & Mace, 2006). Although studies of ancestral condition do not necessarily demonstrate adaptation, they are essential in arbitrating between different causal hypotheses for the origins of cultural traits. For example, if the ancestral Indo-Europeans were monogamous, then monogamy long predates the emergence of Christianity (which is only about 2,000 years old), debunking the common assumption that Christianity is the driving force behind European monogamy. It supports the notion that prevailing local social systems and conventions generally determine religious rules rather than vice versa.

The Puzzle of Low Fertility

Clearly the desire to have children is not hard to explain—it is our raison d'être in evolutionary terms. Evolutionary reasons not to have children, therefore, present a very interesting puzzle to an evolutionary anthropologist or psychologist or demographer. The most obvious phenomenon that curtails human fertility is the demographic transition. Voluntary childlessness and homosexuality are other examples of apparently maladaptive behaviors that clearly reduce lifetime reproductive success, but have been the subject of relatively little research by evolutionary scientists.

The Demographic Transition to Low Fertility

A dramatic and near-universal decline in family size was one of the most pervasive social changes of the past two centuries, and one that continues apace around the world. However there is no clear agreement on how to interpret this demographic transition. Demographers have traditionally placed great emphasis on the reduction in infant mortality as the primary causal factor of fertility decline. There is no doubt it is one driver of the transition to low birth rates, but its failure to predict all aspects of fertility decline lead some to propose cultural transmission of a new idea as a major determinant (Coale & Watkins, 1986). Evolutionary demographers and anthropologists have always focused on high parental investment as key (Borgerhoff Mulder, 1998).

It has long been recognized that maximizing reproductive success is not necessarily about maximizing fertility alone, going back to ornithologist David Lack (Lack, 1954). A “Darwinian demon” that reproduced at the maximum rate is unlikely to succeed in the real world because there will be costs of reproduction to the mother (and probably also to the father), and there will competition between the many siblings for limited parental resources. Trading off these costs with the fitness benefits of fertility is known as a “quantity–quality trade-off,” and is ultimately what we would predict determines the nature of human reproductive decisions. Reproductive rate can coevolve with wealth transfers (such as gifts at marriage or through inheritance), limiting optimal fertility in circumstances when the costs of these transfers is high (Mace, 1998). It is possible that parental investment can snowball, subject to a runaway process driven by competition between individuals favoring quality over quantity of offspring (S. E. Hill & Reeve, 2005; Mace, 2008). This could potentially make competition between siblings for parental investment more intense, not less, in modern societies. However, the reproductive decisions of those of us with small families do not appear to maximize our genetic fitness, despite the numerous social, financial, health-related, educational, and other individual benefits associated with low fertility (Goodman, Koupil, & Lawson, 2012).

If some aspect of society, or indeed any part of a person's environment, has recently changed in ways that would not have occurred before in human evolutionary history, then evolutionary models will not necessarily predict observed behavior; natural selection takes time to work. This is sometimes referred to as “mismatch” or “evolutionary lag.” How quickly individuals respond to changing cues is still relatively unexplored. The society most of us live in has been described as WEIRD: Western, educated, industrialized, rich, and democratic (Henrich, Heine, & Norenzayan, 2010), and the largely urban, industrial, or postindustrial environment where WEIRD societies are found is very different from that in which our ancestors evolved. The very rapid changes in mortality, economy, and nutrition in our recent history has occurred in the blink of an eye on an evolutionary time scale.

Cultural evolutionary models have raised the possibility that low fertility could be the result of prestige-biased copying: In societies in which social success and reproductive success are no longer positively correlated, perhaps due to modern contraception, a predisposition to copying successful people could mean copying low fertility (Boyd & Richerson, 1985). More generally, some cultural evolutionary theorists have argued that models of cultural group selection could ensure that either conformity and/or punishment could lead to the maintenance of cultural differences between groups; competition between these groups could favor cultural behavior that benefits the group (Richerson & Boyd, 2005). Limiting fertility, or any trait that leads to reproductive leveling in groups (such as food sharing), could be an example of a behavior that evolved in this way. In rural Ethiopia, we found little evidence that the decision to start using contraception was spreading by copying friends or family in the immediate proximity or by copying those in your immediate social network, suggesting a limited role for social transmission at this early phase of uptake, although religious affiliation did have an effect (Alvergne, Gurmu, Gibson, & Mace, 2011); this was also the case in rural Bangladesh (Munshi & Myaux, 2006). Meanwhile land inheritance does predict contraceptive uptake in both Ethiopia and Bangladesh, with those with private landholdings to pass on to their children being more likely to use contraception (Gibson & Gurmu, 2011; Shenk, Towner, Kress, & Alam, 2013). This suggests low fertility is coevolving with wealth inheritance as behavioral ecological models predict (Mace, 1998). A dichotomy between explanations based on culture and cost/benefit is somewhat unrealistic. Local cultures impose local costs and benefits, and cultural transmission is one of the ways that humans learn that costs and benefits have changed, or perhaps might change in the future. So costs and benefits and cultural transmission are both important and have complementary effects. The well-known influence of education on women's ^{fertility might be as much a cultural effect as it is an economic effect. It has been argued that education itself enhances the cultural transmission of low fertility norms through populations (Borenstein, Kendal, & Feldman, 2006; Ihara & Feldman, 2004). In villages in rural Poland in the midst of demographic transition, women of similar socioeconomic status have lower fertility in a better-educated village than in a less-well-educated village, providing some support for this view (Colleran, Jasienska, Nenko, Galbarczyk, & Mace, 2014). A preference for wealth and status as achieved by education can thus spread at the expense of fertility, as in this case, but without any evidence that such preferences are maximizing current genetic fitness. If this is some evolutionary lag, natural selection would be predicted to eventually reverse such preferences, but this seems unlikely, so the demographic transition remains something of an evolutionary puzzle.}

How Can Male Homosexual Preference Evolve by Natural Selection?

Male homosexual preference (MHP) is associated with low lifetime reproductive success, but it is too widespread to be understood as something that does not require an evolutionary explanation. It is not often seen as a stable, persistent trait in wild animals. It is occasionally documented in anthropological studies of hunter-gatherers; Hill and Hurtado describe a homosexual phenotype that was rare but observed in Ache hunter-gatherers, of effeminate behavior in males who do not reproduce, but who did not engage in homosexual sex until after exposure to Paraguayans (Hill & Hurtado 1996). Several traditional societies acknowledge the existence of a third gender. It seems the phenotype is too common worldwide to not have been subject to natural selection (2%–6% in Western societies). There is little evidence that homosexual brothers are of direct benefit to their kin by helping them out (Bobrow & Bailey, 2001; Vasey, Pocock, & VanderLaan, 2007); but they may be of indirect benefit to their kin, for example by reducing competition between the other siblings for parental resources. There is good evidence that male homosexuality shows a birth-order effect, with each elder brother (but not sister) significantly increasing the likelihood of homosexuality in males (Blanchard, 2001). Sisters of homosexuals appear to be more fertile than those who do not have homosexual brothers (Camperio-Ciani, Corna, & Capiluppi, 2004). This could be due to shared genetic effects such as feminine beauty (which could, for example, be advantageous to fertility in females but has disadvantageous pleiotropic effects in males). Alternatively this could be simply a side effect of both large family size being heritable, combined with the higher incidence of male homosexuality in younger brothers, but further analysis does suggest a sex-linked sexual antagonistic effect (Camperio-Ciani & Pellizzari, 2012). A model for the evolution of male homosexual preference shows that, in a stratified society, a relatively high frequency of MHP could be maintained as a result of the social ascension (or up-migration through social strata) of females signaling high fertility (hypergyny) (Barthes, Godelle, & Raymond, 2013). Their prediction that MHP is more prevalent in stratified societies was significantly supported in a sample of 48 societies for which the presence or absence of MHP has been anthropologically documented. They argue that any traits associated with up-migration are likely to be selected for in a stratified society and will be maintained by frequency dependence even if they induce a pleiotropic cost, such as MHP. This insight applies to the evolutionary basis of any trait that lowers fertility but increases social upward mobility. This explanation cannot, of course, explain female same-sex preferences, the explanation for which must lie elsewhere. Other evolutionary reasons for childlessness other than homosexuality have not been greatly studied, but may in many cases to be related to failures in mate choice. Ultimately, any evolutionary explanation for a behavior associated with reduced fertility, that is not due to constraints, is either a short-term maladaptive outcome that will only persist long enough for evolution to remove it; or it is a stable feature in a given population and thus can only be explained as an adaptation in evolutionary terms if it is associated with indirect benefits to existing children or other kin.

Conclusions

Human behavioral ecology has proved an essential framework within which to understand human kinship and family systems. Behavioral ecologists start from the premise that natural selection works on behavior to maximize fitness. They use three main approaches to test adaptive hypotheses about the evolution of behavior: experimentation, testing the predictions of theoretical models, and the comparative method (Krebs & Davies, 1993). When a particular adaptive model fails to explain observed phenomena, the usual modus operandi is to seek a better model, assuming that some vital cost or benefit has been overlooked; hence, our understanding of the evolutionary basis of that behavior is enhanced by ruling out multiple alternative explanations. Human behavioral evolutionary studies are often described as falling roughly into three main schools of thought: evolutionary psychology (often experimental studies seeking universal psychological adaptations), gene culture or cultural evolution (generally focused on theoretical models of cultural evolution), and human behavioral ecology (Laland & Brown, 2002). The last two are primarily interested in explaining variation in human behavior. Although sometimes taking different approaches, often generating different conclusions, these fields are becoming similar and sometimes indistinguishable (Mace, 2014).

Family systems have been the traditional obsession of anthropologists since the inception of the field. How families influence our reproductive and other behaviors is now a subject of interest across the full range of human sciences. Understanding the evolutionary basis of human families illustrates the usefulness of a range of evolutionary approaches, as well as the central importance of ecology. Although all human societies base social organization around the building block of families, the nature of those families do vary through history and around the world. I have outlined here how evolutionary ecology provides a framework that can be used to explain a range of phenomena to do with our social organization, reproductive physiology, cultural norms, and parenting behavior, and how they coevolve to generate the diversity that we observe, both within and between cultures, in human family life.

Note

Ruth Mace's research is funded by the ERC (AdG 249347). All the issues discussed have benefited from discussion and collaboration with many people, with special thanks to present and former members of her research group HEEG at UCL Anthropology.

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