PETER B. GRAY*, PH.D., and ALYSSA N. CRITTENDEN*, PH.D. Father Darwin: Effects of Children on Men, Viewed from an Evolutionary Perspective Inspired by Charles Darwin, we explore the evolutionary trajectory of human fatherhood. Paternal behavior is a prominent feature of our species’ behavioral biology, with most models suggesting core features having been derived within the past few million years of evolution. Specific components—holding, provisioning, protecting, providing moral guidance—have evolved in mosaic fashion rather than as a complete package. The impacts of fatherhood on men’s lives take a variety of forms. Becoming a father has impacts on men’s relationship quality, sexual function, neuroendocrine system, and other health-related outcomes. These effects suggest an overall model in which involved fathering of a young child can yield negative health impacts that may subsequently rebound as a child grows older. Keywords: fatherhood, paternal investment, paternal care, life history theory, human evolution A couple of years after Charles Darwin had returned from a five year voyage around the world, encountering new species and contemplating the processes by which species and adaptations arose, he contemplated one of the larger questions in life: to marry or not? He sketched reasons both to marry and reasons not to marry in one of his notebooks (Darwin, 1838). At the top of the reasons to marry was “children (if it Please God).” Other reasons to marry included the benefit of a “constant companion,” one who might be “Better than a dog anyhow.” He recognized the allure of the “charms of music and female chit-chat” and “a nice soft wife on a sofa with good fire and books,” also noting that such benefits of marriage could be “good for one’s health.” On the contrary, his list of reasons not to marry was of comparable length, including concern over the “expense and anxiety of children,” “loss of time,” “fatness and idleness,” and “If many children forced to gain one’s bread (But then it’s very bad for one’s health to work too much).” * University of Nevada, Las Vegas. Correspondence concerning this article should be addressed to Peter B. Gray, Department of Anthropology, University of Nevada, Las Vegas, 4505 Maryland Parkway, Box 455003, Las Vegas, NV, 89154-5003. Email: [email protected] FATHERING, VOL. 12, NO. 2, SPRING 2014, PP. 121-142. © 2014 by the Men’s Studies Press, LLC. All rights reserved. http://www.mensstudies.com fth.1202.121/$15.00 • DOI: 10.3149/fth.1202.121 • ISSN/1537-6680 • eISSN/1933-026X 121 GRAY & CRITTENDEN Whatever the impact of Darwin’s tabulation, he did marry his cousin, Emma Wedgewood. By all accounts, they had a successful and supportive marriage, as well as a reproductively fruitful one. They had ten children, seven of whom reached adulthood. The loss of his beloved daughter Annie, at age 10, was emotionally devastating, one indication of how much his children meant to him. Becoming a father also afforded Darwin with opportunities to study his own progeny, with a natural historian’s eye. In an 1877 essay, he commented on one of his son’s developing moral sense, for example. “The first sign of moral sense was noticed at the age of nearly 13 months. I said “Doddy” (his nickname) won’t give poor papa a kiss—naughty “Doddy.” These words, without doubt, made him feel slightly uncomfortable; and at last when I had returned to my chair, he protruded his lips as a sign that he was ready to kiss me.” Darwin took his children to the London Zoo, where he also contemplated the capacities of apes compared with his own children. He showed an orangutan a mirror to see if it recognized itself in its reflection, also holding a child of his in front of a mirror to test the same ability. This method of self-recognition in a mirror would become a 20th century technique to investigate what psychologists refer to as “theory of mind,” or the ability to attribute mental states to others. The point of beginning this overview of the evolutionary impacts of fatherhood on men with Charles Darwin is to recognize the profound ways that marriage and fatherhood themselves impacted this intellectual giant. Fatherhood shaped Darwin’s day-to-day life at Down House and some of the ways he thought about the natural world. As a father of evolutionary theory, Darwin’s notebook sketch would also point to, as we shall see, some of the nowrecognized impacts of marriage and fatherhood on men (e.g., with respect to time allocation and health). Furthermore, the integrative ways—drawing upon observations of other animals, of people cross-culturally, on the limited fossil record, on demographic concepts—also resonate with how, today, we can undertake a deeper understanding of fatherhood and its effects on men. In the following overview, inspired by Father Darwin, we address two central questions: How did human fatherhood evolve? What are the impacts of children on their fathers? THE EVOLUTION OF HUMAN FATHERHOOD Since Darwin’s foundational work, evolutionary approaches to human behavior have incorporated elements both of phylogeny (evolutionary history) and function (i.e., adaptation) (c.f., Tinbergen, 1963). In this paper, we embed evolutionary scenarios concerning human fatherhood within the specific time frames and contexts of our ancestors, consistent with the importance of phylogeny to understanding the evolutionary history of human paternal care. As we will see, some evolutionary-based aspects of human fatherhood (e.g., protection) have arisen much earlier than others (e.g., wealth transfers). We also attend to functional concerns, recognizing that an individual’s reproductive effort (time and resources designed to enhance success of offspring) may be compartmentalized into mating or parenting effort. It was presumably adaptive for ancestral males to channel their reproductive effort into aspects of parenting effort (e.g., provisioning and direct childcare) rather than (as most mammals do) focus entirely upon mating effort (competing with other males and mating with females). A number of models have been advanced to account for the evolution of human fatherhood. These models incorporate features of both phylogeny and function, and are situated within the kind of integrative evolutionary framework that Charles Darwin had helped establish. A set of these primary models is outlined in Table 1. The empirical foundation for these models is often based on data on the foraging and social behavior of human hunter-gatherers, because although they are not an identical model for Paleolithic behavior, 122 123 Consistent with some elements of male foraging activities, including males targeting widely-shared resources such as large game Linked with emergence of the genus Homo, mapping onto increased metabolic costs and increased body size. Hunter-gatherer data do not support a prominent role for fathers’ protection against infanticide; protection against harassment by others may be a regular benefit of paternal protection No direct benefits to offspring May benefit from male protection and access to a father Offspring benefit from availability of paternal caregiver Provide food resources that are unpredictable and widely shared (i.e. consumed by many) to gain reproductive benefits Males provide protection and are accessible to genetic offspring Males provide direct care of to offspring Male direct care, in the form of Helps shorten inter-birth ininfant carrying, frees energetic tervals constraints on mothers Reduces harassment by other Benefit by reduced harassindividuals and, in the extreme, ment or being killed infanticide Show-off Hypothesis (Hawkes, 1991) Ape Phylogenetic Inertia (Duda & Zrzavy, 2013) Male Direct Care (B.S. Hewlett, 1991, ed., 1992) Energetics and Male Care (Gettler, 2010) Protection (van Schaik, & Dunbar 1990) Consistent with hunter-gatherer data, although the Aka time allocation data by fathers are anomalous compared with other forager societies. Consistent with protection offered by some extant apes such as gorillas, but not with direct care, provisioning or impacts on offspring social development Benefit by male provisioning Relevance to recently studied hunter-gatherers, with implications for aiding maternal energetic in- the evolution of pair bonding vestment Critical Period of Provisio- Increase foraging intensity to ning (Marlowe, 2003; Quin- aid mate during late pregnancy and postpartum lan, 2008) Relevance to recently studied hunter-gatherers, but unlikely to be the starting point of Homo shifts to paternal care Offspring may gain access to greater dietary breadth; provisioning may allow shorter inter-birth intervals Male Provisioning (Lancas- Gain from mating access with a ter & Lancaster, 1983; Ka- long-term partner within a sexual division of labor plan et al., 2000; Lovejoy, 1981) Human offspring require care Forager offspring are raised by mothers and various other caregivers, including fathers, with these patterns likely arising in the genus by others besides mothers Homo; consistent with plasticity in family dynamics; does not emphasize specific aspects of paternal care Provide care that enhances a mate’s lifetime fertility Cooperative Breeding (Hrdy, 2009) Timing and Relevance Offspring Perspective Male Perspective Model Table 1 Models of the Evolution of Human Fatherhood FATHER DARWIN GRAY & CRITTENDEN they do represent a nomadic foraging lifestyle that has characterized well over 90% of human history. Foragers are, therefore, ideal populations in which to study evolutionary aspects of behavior. In the remainder of this section, we discuss some of the core elements of these models and take-home concepts concerning the evolution of human fatherhood. Data on primate behavior and evolution, particularly from extant wild apes like chimpanzees and gorillas, also contribute to inferences about the timing and potential adaptive contexts in which key elements of human fatherhood arose. See Figure 1 for a depiction of 8 7 6 5 4 3 2 1 Millions of years ago Chimpanzees Sahelanthropus tchadensis Bonobos Orrorin tugenensis Ardipithecus Adaptations for walking bipedally, smaller canine teeth Australopithecus anamensis Australopithecus afarensis Feet partially adapted for bipedalism Australopithecus garhi Enlarged cheek teeth and jaws Australopithecus africanus Paranthropus Massive cheek teeth and jaws, enlarged chewing muscles Homo habilis Slightly larger brain (600 cc), more vertical face without a snout, fingers capable of precision grip, ability to make simple stone tools for processing food including meat Homo erectus Smaller jaws and cheek teeth, long legs and arched feet well suited for long-distance walking and running, larger brain (Homo erectus brains range from 650 cc to 1200 cc.) Homo neanderthalensis Homo heidelbergensis Sophisticated stone flakes, tools for hunting, brain size increases to 1200 cc Large brain (1400 cc), small face tucked below braincase, rounded cranial vault, small browridges, capacity for art, symbolic thought, full-blown language Homo sapiens Figure 1. Chimpanzee, bonobo, and hominin phylogeny, also illustrating key evolutionary trends in hominin biology and behavior. Image used courtesy of Ben Roberts, of Roberts and Company Publishing, and reproduced from “The Tangled Bank: An Introduction to Evolution”. 124 FATHER DARWIN a hominin phylogenetic tree. Hominins are humans and close (but extinct) relatives since splitting off from a last common ancestor with chimpanzees and bonobos approximately six million years ago. Data from the fossil and archaeological record can help in specifying details of the timing and directionality of evolutionary change, including changes in brain size among our hominin ancestors. Genetic and physiological data can speak to potential heritable bases of paternal behavior, of the proximate mechanisms governing the expression of paternal behavior, and of the consequences of antecedent reproductive behavior. Helping organize these multiple lines of evidence are general evolutionary theoretical principles, such as sexual selection theory, a body of work that helps account for how reproductive competition can shape anatomy, physiology and behavior (Darwin, 1871; Geary, 2010). To illustrate, the larger (compared with females) human male upper body musculature and oxygen-carrying capacity are thought to have been favored by sexual selection in the context of ancestral male-male physical aggression (fighting). In light of these various lines of evidence, a critical evaluation of various theoretical models will increase our understanding of the evolutionary foundations of human fatherhood. Fossil evidence of increases in cranial capacity and decreases in body size dimorphic indices across hominins suggest that many aspects of cooperation, in general, and paternal care, in particular, may have evolved with the genus Homo. While Figure 1 notes that brain sizes increased among our hominin ancestors predominantly within the past two million years, other evidence suggests that body size sexual dimorphism (which can be an index of mating competition, with larger males favored for fighting other males) also decreased within the past two million years (see Flinn et al., 2005; Gray, 2013). Cooperative breeding (or child rearing), mate selection, and direct paternal investment have been linked with many key milestones in human evolution such as family formation, pair bonding, and routine food sharing (Lancaster & Lancaster, 1987; Lee & DeVore, eds., 1968). To illustrate, Lee and Devore feature discussions of male hunting among foragers, how those resources garnered by males may be exchanged with a mate within a familial sexual division of labor, and how the resources provided by fathers (and mothers) are central to raising children. In the next section, we discuss how human fatherhood can be situated in a mammalian evolutionary framework, incorporating elements of both phylogeny and function, and then in subsequent sections we discuss how specific aspects of male fatherhood arose at different times. Cooperative Breeding, Mating Effort, and Pair Bonding The evolution of human fatherhood is best viewed against a theoretical and empirical backdrop of mammalian reproduction, in general, and male reproductive effort, with an emphasis on mating effort, in particular (Royle, Smiseth, & Kolliker, eds., 2012). Human reproduction is characterized by features that distinguish it from the general mammalian pattern and from the pattern seen among apes—our closest living relatives. Humans are distinct in that we wean our infants before they are nutritionally independent and we have relatively short inter-birth intervals (IBI)—the space between births (Kaplan et al., 2000). Early weaning allows a mother to resume ovarian cycling more rapidly—effectively shortening the IBI and permitting mothers to give birth to new infants while maintaining care for older, and still highly dependent, children. This ability to “stack” infants, while making humans incredibly reproductively successful, has serious reproductive consequences for a mother, as children require high degrees of behavioral and nutritional investment for lengthy periods of time. 125 GRAY & CRITTENDEN It requires approximately 13 million kilocalories to raise one infant from birth to nutritional independence, and such requirements exceed what a mother can produce alone (Hrdy, 2009; Kaplan, 1994). How does a human mother meet the challenge of providing for herself and multiple dependent offspring? Increasingly, cross-cultural data suggest that mothers meet this reproductive challenge by relying on the assistance of other group members, allomothers, who provide care for and/or provision her children. This dependence on external support is considered to be a hallmark of human evolution, identifying humans as “cooperative breeders” (Hrdy). Cross-culturally, a wide range of helpers provides high quality care (Kramer, 2011), yet two categories of helpers consistently stand out as critical: grandmothers (Hawkes & Coxworth, 2013) and fathers. While fathers represent a key category of helper, their contributions vary widely within and between populations (Gray & Anderson, 2010). Fathers may have been central to infant survival during the Pleistocene (Lancaster & Lancaster, 1989; Lovejoy, 1981) and emergence of the genus Homo (Bribiescas, Ellison & Gray, 2012). This proves to be another unique characteristic of human reproduction, as human males are among the mammalian minority where parental care is a regular feature of male reproductive effort. Across mammals, approximately 3% (Kleiman, 1977) to 10% (Lukas & Clutton-Brock, 2013) are socially monogamous, with a fraction of those species also displaying significant amounts of direct and indirect paternal care. Put another way, across most species of mammals, males focus their reproductive effort entirely on mating effort, competing with other males to mate and seeking to coerce or attract a female willing to mate with him. Humans are among the minority of mammalian species with long-term reproductive bonds, though these are best characterized as slightly polygynous/mostly monogamous rather than strictly socially monogamous (Gray & Garcia, 2013). Put in this light, the allocation of male reproductive effort toward long-term bonds and offspring entails a reduction in aspects of mating effort (that is, entails less male-male physical competition and courtship of mates). That is an important way to conceptualize many of the effects of children on fathers, as we shall see. That is also distinct from a standard that compares males with females on measures such as direct parental care, viewing a 50:50 split as some targeted ideal. However, this standard of sameness is often implicitly, if not explicitly, employed when evaluating human paternal care. Fathering cannot be easily disentangled from reproductive bonds. Most human reproduction takes places within the context of long-term partnerships that can be recognized as marriage (Gray & Garcia, 2013). That is true among hunter-gatherers, but not among most monkeys and apes (Dixson, 2012). While gorillas form long-term polygynous reproductive relationships, chimpanzees, bonobos, and orangutans do not. The implication is that future fathers are chosen with respect to their abilities to function within long-term partnerships, valuing abilities to serve as a viable provisioner and to display other characteristics indicative of long-term compatibility. Wider evolutionary principles also apply to this connection between long-term bonds and paternal behavior. Comparative research on other mammals and primates indicates that long-term bonds are best viewed as a necessary, but insufficient, predictor of paternal behavior (Lukas & Clutton-Brock, 2013). An implication is that the evolutionary origins of human ancestral reproductive bonds likely preceded paternal behavior. While there is not a consensus on the factors underlying the origins of long-term reproductive bonds among human ancestors (Gray, 2013), leading models would point toward male mate guarding of females and females acceding to such guarding in light of costs/benefits (e.g., in reduced coercion of offspring by others), with central aspects of direct and indirect paternal care later derivations. Another key point from the linkage between long-term 126 FATHER DARWIN reproductive bonds and paternal care is that human paternal care is best viewed as, at minimum, a triadic phenomenon: involving a father, a mother, and their child. This triadic relationship lies at the center of several key evolutionary models of fatherhood. MALE PROVISIONING Perhaps the most prominent model of the evolution of fatherhood is some variant of a “Man the Hunter” portrayal, with that label tracing to a 1968 edited volume of the same title in which several contributions highlighted the primary role of male provisioning among hunter-gatherers (Lee & Devore, eds., 1968). The basis of such male provisioning models is that males obtain high quality food resources, particularly meat obtained by hunting, which they share with their mate in a sexual division of labor and use to provision their children. A male provisioning model has several key merits. One is that studies of recent foragers lend support to these features of male resource acquisition and sharing within a sexual division of labor. Some scholars, such as Kaplan et al. (2000) and Wood and Marlowe (2013), provide quantitative data on estimated male caloric contributions. Studies of extant apes evidence very little food provisioning or a sexual division of labor (Mitani et al., eds., 2012), also suggesting that male provisioning and a sexual division of labor were derived relatively recently in human evolution. Male provisioning models have also been challenged, however, using data on male food contribution in extant foragers. Hawkes (1991) introduced the “show off” hypothesis, based on data collected among Hadza hunter-gatherers, and proposed that males seek unpredictable resources, such as large game, as a means of “showing off” to potential mates. Rather than targeting resources to provision their families, she contends that male foragers instead focus on resources that amount to “public goods” when widely and openly shared. Males target those goods to advertise mate value or gain reproductive benefits, such as acquiring an additional wife or extra-pair sexual partner. One extension of the “showing off” model is that male hunting prowess can be viewed as “costly” or “honest signaling” under the idea that male hunting ability may be an indicator of his general “quality” in addition to being of economic importance (Bird, Smith, & Bird, 2001; Hawkes & Bird, 2002). Rebuttals to “showing off” or “costly signaling” models also present data collected among Hadza foragers to suggest that men routinely target other, more dependable resources (e.g. honey, fruit, and small game) that are preferentially shared with wives and children rather than across an entire camp. Detailed study of game meat sharing by Wood and Marlowe suggest that, even for large game, families may disproportionately benefit (Wood & Marlowe, 2013). The summary of these points is that male resource acquisition and sharing strategies among foragers represent a combination of mating effort and parenting effort (Geary, 2010). Males may partly target resources to garner a positive reputation that in turn grants them other reproductive benefits, but male provisioning models also have clear support. As an additional extension, Marlowe (2003) suggests that male provisioning is most important during the “critical period” of a mate’s late pregnancy and early postpartum lactational states when her foraging efficiency may be compromised. By this view, the importance of male provisioning fluctuates across reproductive bouts. Most male provisioning models do not specify the evolutionary time frame over which they are presumed to have operated. As an early and important exception in this vein, C. Owen Lovejoy (1981) contended that male provisioning arose among Australopithecus ancestors approximately four million years ago in Africa as part of the evolution of a sexual division of labor, long-term reproductive bonds, and concealed ovulation. More recent finds 127 GRAY & CRITTENDEN of Ardipithecus, an early hominin have led Lovejoy (2009) to effectively recast similar claims about a role of male provisioning and a sexual division of labor originating around five million years ago in Africa. However, several lines of evidence argue against such an early origin of male provisioning among human ancestors. The archaeological record of stone tools and butchered animal bones, which could be linked to male provisioning models, originates and becomes more prominent from around 2.5 million years ago to the present (rather than an earlier time frame) (Lieberman, 2011). The degree of putative body size dimorphism (differences in body size between males and females) among these earlier hominins is subject to dispute (Plavcan, 2012), but most scholars infer a higher degree of dimorphism that would argue against social monogamy and provisioning among early hominins or Australopithecus (e.g., Flinn et al., 2005). Inferences about development (e.g., duration of infancy and juvenility) based on extant apes, human hunter-gatherers, and dental data suggest changes within the genus Homo in the past two million years in concert with other factors such as greater paternal care rather than at some earlier time (e.g., Thompson & Nelson, 2011; Meehan & Crittenden, under review). Furthermore, general evolutionary principles argue against an immediate effect of male provisioning driving long-term reproductive bonds (rather than being subsequent developments) (Reichard & Boesch, eds., 2005). While such lines of evidence more plausibly point to male provisioning arising within the past two million years in the genus Homo, this body of work also suggests male provisioning as observed among foragers is the product of multiple antecedent economic and social steps. The earliest evidence of spears traces to approximately 500,000 years ago in Europe, the earliest evidence of arrows less than 100,000 years ago in South Africa, but such technologies likely had significant influences on male provisioning potential once adopted, also meaning that foraging data from today’s hunter-gatherers likely do not project well to much earlier dates (see Marlowe, 2005). Observations in the fossil record that estimated brain sizes increase in several grades during the genus Homo (early Homo about two million years ago; so-called Homo heidelbergensis around 600,000 years ago; with modern humans 200,000 years ago) and that developmental schedules also appear to reflect similar patterns of grade shifts (i.e., in extended periods of juvenility and later age of sexual maturity) suggest mosaic evolution in our ancestors’ social behavior the past two million years (Foley & Gamble, 2009; Lieberman, 2011). Additional inferences are that paternal behavior likely contributed to those changes, and that the full package of behaviorally modern humans arose with, literally, the origin of modern humans 200,000 years ago in Africa. MALE PROTECTION In contrast to models featuring male provisioning, the relevance of male protection to offspring well-being and survival is more difficult to specify. Much of the controversy surrounds a putative role for male protection in infanticide avoidance (Hrdy & Hausfater, 1984; Palombit, 2012). Without a father’s protection, might ancestral infants have been subject to killings by unrelated males? Data on wild gorillas suggest a sizable fraction of infant deaths trace to infanticide (Watts, 1989), itself related to the death of or possible overthrow of a dominant reproductive male gorilla by another adult gorilla male. While some scholars suggest a functional role of male protection against infanticide in gibbons and siamangs (van Schaik & Dunbar, 1990), alternative interpretations of male-female socially monogamous bonds in these species emphasize food defense and mate guarding (Reichard & Boesch, eds., 2005). In a jolting contention, based on characterizations of social behavior of extant 128 FATHER DARWIN apes and some monkeys, Duda and Zrzavy (2013) suggest that an ancestor to all apes (from gibbons to orangutans to gorillas) and humans had evolved paternal care, meaning that it would have appeared and been maintained approximately 20 million years ago. Closer analysis of their claim rests on the coding of “paternal behavior,” with the view that they collapse multiple behaviors—such as the defense offered by gorilla fathers, the accessibility afforded by gorillas and gibbons to their young, and offspring carrying by siamangs— under this one label. Their contention has more merit and relevance to discussions of paternal protection. While it is difficult to reach definitive conclusions about a role for paternal protection against infanticide among early apes or early hominins, the human huntergatherer literature does not support a view that this is of much adaptive significance (Daly & Wilson, 1988). While children in a few foraging societies, such as the Ache (Hill & Hurtado, 1996), are subject to increased risk of being killed if their father dies, most infanticide among hunter-gatherers is practiced by mothers rather than other males. At a lesser degree of severity, however, it may be reasonable to suggest that fathers help deter harassment (even if that does not result in intentional killing by an unrelated individual) of their offspring by others. In several species of monkeys living in multi-male, multi-female groups, fathers sometimes protect their offspring against harassment (Muller & Emery Thompson, 2012). It is also reasonable to suggest that hominin fathers have long offered protection against predators such as large cats in addition to menacing members of their own species, although it is difficult to quantify or trace the time depth of paternal protection against predators. Direct Paternal Care, Offspring Social Development, and Shared Wealth Several models emphasize the relevance of direct care among fathers. Direct care refers to behaviors such as holding or carrying offspring (Kleiman & Malcolm, 1981). Quantitative time allocation data on human hunter-gatherers show that fathers in several societies, such as the Hadza, devote around 5% of waking hours to such activities, whereas comparable data among the Aka indicate much higher direct care contributions by fathers (B.S. Hewlett, 1991). These data pale in comparison to direct care by mothers, and often with respect to others, such as grandmothers or older siblings (e.g., Crittenden & Marlowe, 2008; Meehan, 2005; Kramer, 2005). These data also pale in comparison with the efforts of some South American monkeys, such as owl monkeys, titi monkeys, tamarins and marmosets, put into carrying or holding offspring (Bales & Jarcho, 2013; Fernandez-Duque, Valeggia & Mendoza, 2009). As an example, titi monkey fathers often carry infants on their backs during travel, handing them over to the mother for lactation. Compared with great apes, however, human hunter-gatherer fathers devote a higher percentage of their waking hours to direct care. The differences are even more pronounced when considering that huntergatherer fathers tend to sleep near their children; given night waking patterns, fathers may face additional, night-time interactions with their young children that are not captured in the available time allocation data. Such patterns suggest that human fathers’ direct care contributions have been derived during hominin evolution. Various considerations, like those touched on above, that point toward several grade shifts in hominin social behavior in the past two million years of Homo evolution would also suggest enhancement of direct paternal care during those time frames. Moreover, direct paternal care could serve multiple functions. It may facilitate paternal attachment to an offspring. It may contribute to offspring social development. It may alter maternal energetics (e.g., male carrying can reduce the energetic burden placed upon mothers during foraging; Gettler, 2010). Direct male care may 129 GRAY & CRITTENDEN also enable more efficient foraging behavior (e.g., by a father babysitting a slow-moving toddler while the mother forages). Consequently, the impacts of direct paternal care on maternal energetics may help allow more rapid resumption of ovarian cycling after having given birth, in turn contributing to shortened IBIs (Gray & Anderson, 2010). Fathers are also likely to impact offspring social development (Lamb, ed., 2010; Leidy, Schofeld & Parke, 2013). Observations of father-offspring interactions in great apes indicate that gorilla fathers may be accessible to their offspring, allowing them to play on or around them. However, there does not seem to be much active social engagement by gorilla fathers with their young, and no formal teaching has been described (H. Smith, 2005). Among hunter-gatherers, fathers’ presence and direct care ensure that fathers are regular features of their children’s upbringing. As their sons develop more independence during mid-childhood and through adolescence, fathers may facilitate sons’ acquisition of sex-specific foraging skills. How fathers impact sons’ (or daughters’) social development more specifically is difficult to discern, however. One foundational evolutionary and developmental model suggests that father absence/presence might serve as a social cue to children’s subsequent social and reproductive behavior (Draper & Harpending, 1982). Under this model, the regular presence of a father through years of dependency (i.e., around age 5-7) would serve as a social indicator that social life affords consistent support and relative stability (and thus channel an offspring’s later reproductive effort more toward parenting effort), whereas the absence of a father would connote greater social uncertainty (and thus channel an offspring’s later reproductive effort more toward mating effort). Among huntergatherers, divorce rates have been quantified in several societies (Blurton Jones et al., 2000). Variation in divorce rates could contribute to differential father absence/presence, particularly since divorces are most prevalent during early adulthood (Winking et al., 2007). One last category of human paternal care that has arisen within the past 10,000 years is non-food resource provisioning, or wealth transfer (Gray & Anderson, 2010). Fathers may provide land, livestock, or other stores of wealth to their offspring, whether during life or upon death. Since these heritable stores of wealth are thought to have emerged with complex foragers and with the domestication of plants and animals, and are absent among extant apes, this component of paternal care has a shallow, yet relevant, evolutionary history. As an illustration of resource provisioning, in societies with brideprice, in which resources such as cattle may be required in the negotiation of a marriage, the ability of a father to contribute such resources to a son may impact the age at which his son is able to marry and begin a reproductive career. SUMMARY OF CONCEPTUAL POINTS: THE EVOLUTION OF HUMAN FATHERHOOD After having laid out and discussed some of the most central models outlining the evolution of human fatherhood, what are the key points of this endeavor? One important point is that fatherhood is not a uniform phenomenon. An attempt to assign a single label, such as identifying the presence or absence of paternal care or forcing the distinction between mating effort and parenting effort, across species masks the heterogeneous processes that collectively make up paternal care. Duda and Zrzavy’s (2013) paper illustrates this point well as, contrary to all other models, they infer paternal care among all apes, and claim more ancient evolutionary roots to paternal behavior. Instead, paternal care consists of a set of distinct components: direct care; indirect care (food provisioning, protection, wealth transfers); and social and moral training (Gray & Anderson, 2010). Moreover, the relevant evolutionary context shaping these respective components varies. Protection against ha- 130 FATHER DARWIN rassment may have the deepest time depth, while food provisioning, direct care and social and moral training likely underwent several shifts during the past two million years of Homo evolution. Wealth transfers are of most recent evolutionary history. These patterns mean that the evolution of human paternal care arose in mosaic fashion—piece by piece at different time frames—rather than as a package. Moreover, changes in the social and institutional settings in which human paternal care is expressed have been, and continue to be, highly variable. The variable influences of formal education, religions, and other institutions have usurped many of fathers’ social and modeling influences, compared with hunter-gatherer societies, with protection also variably co-opted by other institutions. An evolutionary perspective suggests that the most salient impacts of paternal care are on enhanced fertility and offspring social development, rather than on offspring survival (Gray & Anderson, 2010). The impacts of male provisioning and direct paternal care may manifest in offsetting the energetic constraints on female reproductive function (see Ellison, 2001). Across foragers, Marlowe (2001) showed that the greater the male contribution to subsistence, the shorter the inter-birth interval, consistent with male care enabling higher human fertility. Fathers may also impact the social development of children, with some sexspecific effects. Yet studies that have investigated effects of father death on offspring’s mortality have found quite mixed effects: in about half of studies that used appropriate statistical analysis, the death of a father was not associated with any mortality difference on offspring, whereas in the other half of societies it was (Sear & Mace, 2008). By contrast, in every society in which a mother dies, her offspring suffer higher mortality, and in a higher fraction of societies the death of a grandmother was more often associated with offspring death compared with father deaths. The implication is that effects of male care may be less apparent in survival than those other aspects of paternal care. All models of human fatherhood tend to feature prime-aged genetic fathers at the expense of greater variation among fathers. As one important element of that additional variation, the data on hunter-gatherer divorce and death suggest that children have long grown up within families of mixed parentage, including the presence of stepfathers. Marlowe (1999) showed that, among Hadza foragers, stepfathers scored lower on several measures of paternal care compared with genetic fathers. Such differences are consistent with kin selection theory (Anderson et al., 1999; Hamilton, 1964). However, the investment by stepfathers can be viewed as mating effort, designed to entice sexual access to a child’s mother in whom the man invests (e.g., Smuts & Gubernick, 1992). Compared with other apes, human fathers also display less reproductive skew (variation in reproductive output) and older ages of fathering offspring (see Brown et al., 2009; Mitani et al., eds., 2012). The lower reproductive skew is consistent with more even reproductive distributions across males (e.g., more men reproducing, and having more similar number of offspring, compared with chimpanzees), and claims that humans are a relatively egalitarian species (Boehm, 1999). The later ages of male fathering, in part, occur because of the long-term relationships in which humans tend to reproduce, allowing some hunter-gatherer men to reproduce well into middle age with younger wives and also father offspring at ages, by which all other wild great ape males would be dead. In addition, variation in male “quality” has been recognized among foragers, highlighting variation in hunting reputation or shamanic ability, also with reproductive consequences to the differential status that it confers (E. Smith, 2004). The key is that variation underlies typological characterization of any one aspect of paternal care, and this extends to the above discussion of evolutionary models. If some ancestral men’s provisioning was part of an emerging hominin paternal contribution, there was assuredly variation then, as there is presently, in how men performed in that arena. 131 GRAY & CRITTENDEN THE EFFECTS OF CHILDREN ON FATHERS Having considered the evolutionary backdrop to how human males came to care for their children, let us now turn to the question of what effects children have on their fathers. In this section, we devote less space to hunter-gatherers, and instead turn to a wider array of social contexts in which paternal care manifests. Although data on the effects of children on huntergatherer fathers, or fathers in other small-scale societies, would be welcomed, such data are in relatively short supply. However, data on fathers in countries like the U.S., sometimes employing large samples, are more readily available. We also focus on central concepts and illustrative data in discussing these transitions given space limitations, noting that readers can find additional documentation of the key effects noted below in other references (e.g., Astone & Peters, 2014; Eggebeen et al., 2013; Gray & Anderson, 2010; Settersten & Cancel-Tirado, 2010). That said, most of the following emphasis is on the transition to first-time fatherhood, with less attention given, in part because of less available information, on variable effects on stepfathers, or with respect to other key factors such as parity (number of children), age of children, or age of fathers (see Bornstein, ed., 2002; Cabrera & Tamis-LeMonda, eds., 2013). As men become fathers, this may have impacts on the ways in which they spend their time, with those ways quantifiable with time allocation data. Especially for first-time fathers, their involvement in childcare may rise from almost nothing to whatever minutes or hours they spend with or accessible to their newborns. Among men in four subsistence societies(the Efe foragers of East Africa, the Kipsigis agropastoralists of Kenya, the Madurese agriculturalists of Indonesia, and the Machiguenga horticulturalists of lowland Peru), fathers spent more time in childcare, more time engaged in commercial activities, less time in education, and less time chatting compared with non-fathers (Gray & Anderson, 2010). Research on men’s work hours shows that any impacts tend to be relatively modest, as Gauthier and Furstenberg Jr. (2002) observed among large samples of fathers drawn from nine countries, including Italy, Canada, and the U.S. In some studies, men’s work hours increase slightly after having a child, in a way that may resemble the “critical period” model previously articulated among hominin forebears. In other cases, men’s work hours remain virtually the same. Paid childcare leaves may lead to some short-term decreases in men’s work hours immediately after a child is born, but these are small contributions to the overall picture. Indeed, the relative consistency in men’s work hours after having a child makes sense when viewed from a standpoint of paternal provisioning. Men continue to provide resources, whether through a salary or other means, that were part of what made them eligible as mates in the first place, and that help enable them to contribute to a new child. If men face other shifts in time allocation after having a child, several other facets of these shifts in time allocation stand out. In a nationally representative U.S. probability sample, men who became fathers experienced decreases in overall socializing and leisure time (Knoester & Eggebeen, 2006). Across societies, among those small-scale societies in which warfare had been more prevalent, male-male relationships may have been at a greater premium to aid in defense and raiding, with those thus privileged in contrast with other societies in which direct paternal care (rather than male-male relationships) was more marked. In some national data, however, men’s leisure time spent with other men may decrease with entrance into a long-term relationship such as marriage, consistent with a large 1960s dataset drawing upon twelve countries (Szalai, 1972); those have tended to be samples in which marriage was closely followed by fathering a child, but also suggesting the importance of marriage, per se, as pushing in that direction even before having children. In a related vein, 132 FATHER DARWIN and perhaps partly because men’s time allocation is shifting in male-male leisure across marriage and fatherhood, men’s risky behavioral profile may be altered (Eggebeen et al., 2013). Married men in the U.S., for example, evidence lower rates of alcohol abuse, drug use, pathological gambling, and involvement in same-sex homicide. The effects are more measurable with respect to relationship status than fatherhood status, once again indicating the importance of the long-term relationships in which men tend to become fathers helping set a stage for a paternal transition. Of effects directly following fatherhood, a study in Sweden found that long-term cohabitating fathers had lower mortality risk attributed to addictions and external violence, but not traffic injuries or suicides compared to long-term cohabiting childless men. In the U.S., men’s involvement in other organizations may increase, as has been shown for involvement in religious groups, school boards, and kids’ sports organizations among fathers (Eggebeen et al., 2013). The idea here is that fathers seek additional support in which to raise their children, particularly with respect to a social and moral environment in which they would like their children to develop. Men’s relationship dynamics are often altered in the process of becoming fathers. In metaanalysis, men’s reports of marital quality decline in the wake of becoming a father (Twenge et al., 2003). In some studies, these effects can be shown longitudinally, meaning that the differences are not just due to some diminishment of marital quality over time regardless of parenthood (e.g., Cowan & Cowan, 1992; Doss et al., 2009). Cross-sectional studies from several other cultural contexts suggest these may be quite general patterns; in a large Chinese sample, fathers in free-choice marriages reported lower marital quality (Pimentel, 2000), although data from small-scale societies, much less hunter-gatherers, are lacking. As to why marital quality might decline among fathers, this can be viewed as part of a relationship dynamic in which a partner’s attentions may shift from her engagement in mating effort to parenting effort, prioritizing her investment in their offspring over her partner. It can be argued that men tend to gain more emotional benefit from involvement in supportive partnerships than do women. Men’s involvement in an emotionally supportive partnership may offer some removal from the male-male competitive arena, and men may have fewer emotionally supportive outlets than women. Such a view is situated within the conceptual framework of men’s involvement in family life representing a reduction in mating effort. As a child is born, however, a father may lose some of that same emotional support as the relationship dynamic shifts, contributing to reductions in marital quality. Men’s sexual function can be impacted by fatherhood (Gray & Garcia, 2013). Several studies have investigated potential changes in men’s libido across the transition to fatherhood, finding that decreases occur in a sizable fraction of men (reviewed in von Sydow, 1999). As a behavioral measure of libido, masturbation rates assessed in several studies, including a large German sample (von Sydow et al., 2001), did not differ across the transition to fatherhood. However, other research indicates general declines in various measures of sexual behavior across pregnancy and into the postpartum phase, particularly among lactating women (Brewis & Meyer, 2005; Escasa-Dorne et al., 2013; Ford & Beach, 1951). These studies are best understood by beginning with the physiological shifts women experience during pregnancy and with the care of an infant. Those effects in women can be conceptualized as a tradeoff between current and future reproduction; that is, with women’s physiology and behavior oriented toward investment in a gestating fetus or infant rather than the processes of conceiving another child (Escasa-Dorne et al., 2013). The baseline levels of estrogens among non-cycling postpartum, lactating women, as one example consistent with this framework, may make vaginal lubrication more difficult, and thus intercourse more painful. Since most of human reproduction tends to occur within long-term 133 GRAY & CRITTENDEN partnerships, however, the downregulation of women’s libido and other sexual concerns during this peripartum transition can impact a father’s sexual function. He may also experience declines in coital frequency during this peripartum period in concert with his partner’s changes. However, because the effects on father’s libido are more variable and less pronounced than those on mothers during this transition, sex differences in sexual desire magnify, creating potential conflicts over sexuality. In that vein, it may be worth noting that, in their classic work on the human sexual response, Masters and Johnson (1966, p. 168) commented, “Six weeks before and six weeks after delivery usually are proclaimed restricted periods by medical interdiction. Many male partners first break marital vows during this three-month period.” Furthermore, some young Aka hunter-gatherer men as well as most agriculturalist Ngandu men in Central Africa Republic also stated that this would be a time when they would seek an additional sexual partner (B.L. Hewlett & B.S. Hewlett, 2010). The psychological effects of fatherhood can vary (Chin et al., 2011; Palkovitz, Copes & Woolfolk, 2001). That variation may represent pre-existing influences as well as the variable circumstances in which parents find themselves situated. Fatherhood, for many men in many circumstances, serves as a validation of manhood, part of what can make it satisfying and rewarding. In many smaller-scale societies, in which reproduction is normative, a male may not be viewed as a man until he has fathered a child (e.g., Gilmore, 1990). Conversely, impending or realized fatherhood can yield a wider mixture of emotions, including anxiety, distress, and even depression. In one Internet-based sample of fathers of young children, men’s positive and negative affect were positively associated with each other, suggesting that fathers can feel both ways (rather than leaning in one direction or the other exclusively) when caring for a young child (Durette et al., 2011). In light of growing appreciation that postpartum depression can hit fathers as well as mothers, more research is available on this particular psychological outcome than others. In a recent meta-analysis of paternal depressions, Paulson and Bazemore (2010) found that 10.4% of fathers of young children were depressed, with slightly higher rates 3-6 months postpartum compared to earlier or later times. Paternal postpartum depression was correlated (r = 0.31) with maternal postpartum depression, yielding the best predictor thus far identified of paternal postpartum depression. That could be for several reasons, including shared environments (e.g., of poverty), or that men’s emotional states are sensitive to the (depressed) cues of their partners. Data on postpartum paternal depression are lacking from small-scale societies, leaving it an open question whether the observed effects from largely western samples generalize more broadly or not. In light of conceptual shifts in male reproductive effort, alterations in time allocation, changes in relationship dynamics, including sexual function, and alterations in psychological states, what is happening “under the skin?” This is a question, in other words, of the potential physiological effects of fatherhood on men. Virtually all of the relevant human research has emerged since 2000, marking a new area of scholarship on fatherhood. Studies investigating brain imaging (e.g., alterations in brain activity when a father looks at a photo of his child or hears infant cries) and hormones (e.g., intranasal sprays of a peptide hormone, oxytocin, or measuring salivary testosterone) provide insight into the effects of children on men’s bodies (Gray & Anderson, 2010; Rilling, 2013). Much of the research on male testosterone and family relationships has been conceptualized with respect to variable allocation in male mating and parenting effort (e.g., review in Gray & Campbell, 2009; and see van Anders this volume). A large, longitudinal study situated in Cebu City, Philippines, demonstrated that becoming a father decreased men’s testosterone levels, with decreases 134 FATHER DARWIN largest among fathers providing more childcare (Gettler, McDade, Feranil & Kuzawa, 2011). Several studies have investigated both men’s baseline and reactive prolactin levels to paternal status or stimuli. As examples, Gettler, McDade, Feranil and Kuzawa (2012) found, for the first time in humans, that fathers of young children in the Philippines had higher baseline prolactin levels than non-fathers. However, results vary whether fathers’ prolactin levels increase or decrease in response to infant stimuli such as interactions with one’s child (e.g., Gray et al., 2007; Gettler, McDade, Augustin & Kuzawa, 2011). Several studies involving intranasal oxytocin sprays, which are thought to reach the brain and thus exert “central” effects, suggest small paternal behavioral effects relative to placebo in standardized lab studies (e.g., Weisman et al., 2013). In regard to brain imaging, the handful of relevant studies has been conducted largely by James Swain, James Rilling, and colleagues (reviewed in Rilling, 2013; Swain et al., 2007). Among findings in these studies, men listening to cries from their own infants experienced increased activation in several brain areas including the hypothalamus, hippocampus, midbrain and anterior cingulate. These patterns of neural activity suggest roles in long-term memory and social orientation, among other processes. In a study that was unique for combining brain imaging, hormone measurement, and even testicular size measurement, Mascaro, Hackett and Rilling (2013) drew upon a sample of fathers in Georgia. They found that fathers’ variation in ventral tegmental area activation was positively associated with a measure of their paternal behavior. Additionally, ventral tegmental area activation was negatively associated with relative testis size, meaning that fathers with smaller testicles tended to engage in more paternal behavior. Blood testosterone levels were also negatively correlated with paternal behavior. This study suggests that variation in parenting efforts in a sample of fathers of young children was associated with physiological measures of mating and parenting. If fatherhood can have physiological impacts, how does it influence health outcomes such as morbidity (illness) or mortality (death) (Garfield, Clark-Kauffman & Davis, 2006; Gray & Anderson, 2010)? A body of research suggests that marriage differentiates various healthrelated behaviors such as men’s physical activity levels and diet, as well as related measures such as body mass index (BMI). There may be additional, incremental impacts of fatherhood, particularly with respect to sleep. In a prospective Australian study of men becoming fathers, fathers of young children showed declines in health, in part attributed to sleep disruption and psychological distress (Condon et al., 2004). A large Dutch study found that fathers in their 20s had higher waist circumferences but not BMIs compared with nonfathers, with those fathers also less physically active (Nielsen et al., 2007). Generally, however, metabolically-related measures in countries like the U.S. and Australia suggest that most influences begin with involvement in long-term partnerships, with fatherhood adding relatively little to those influences. Such a view draws upon wider discussions of a sexual division of labor (e.g., of activities such as food preparation and healthcare, in which males tend to have lower standards and investments) and time allocation studies (e.g., those showing reductions in leisure activities with other males, some of which could include team sports participation). In several U.S. and Australian studies, self-reported health status suggested that fathers of young children experienced health insults that might release as those same children grew older (e.g., Bartlett, 2004). The health challenges of carrying for a highly dependent offspring may have physiological effects capturing potential alterations in sleep, influences of infectious disease exposure (e.g., from vulnerable offspring to parent), and impacts of relationship and mood alterations, among other effects. But as those same children become more independent, those same challenges (and their respective physiological impacts) may lessen. 135 GRAY & CRITTENDEN At a more fundamental level, how do children impact men’s mortality? As a preface to addressing that question, it is worth noting that human males tend to die at higher rates than females in most samples across the lifespan, including before birth, and extending into advanced ages when demographic skew (e.g., far more older females than males) can be most pronounced (Kruger & Nesse, 2006). The magnitude of human sex differences in mortality profile is consistent with slight polygyny when viewed in comparison with other species of mammals and birds, by which socially monogamous species tend to have more similar male:female mortality profiles, and by which greater male mortality risk occurs the more polygynous a species (Clutton-Brock & Isvaran, 2007). Across various countries, including the U.S., married men tend to live longer than unmarried men, or men who divorce (Hu & Goldman, 1990; Kruger & Nesse, 2006). Some longitudinal studies suggest that part of that difference can be causally attributed to effects of marriage rather than or in addition to effects of pre-existing variables such as healthier men being more likely to marry. In studies that have investigated potential effects of paternal status or fertility on male mortality— rather than marriage—the results have been mixed. While studies of British peerage and Finnish men did not find any differences in mortality rate between fathers and non-fathers, a nationally representative probability sample of U.S. men did observe lower mortality rates among fathers (K. Smith & Zick, 1994). An interpretation of these data on male mortality is that, like for other variables, involvement in a long-term relationship has a more powerful influence than fatherhood per se, but until quite recently in evolutionary history these social contexts were connected (i.e., barring infertility, in a natural fertility population the formation of a long-term sexual relationship would be followed by child-rearing). In that vein, it once again makes sense to situate human paternal experiences as a triadic (father, mother, offspring) phenomenon rather than look to an isolated effect of fatherhood. CONCLUSION In addressing two central questions—how did human fatherhood evolve, and what are the effects of children on fathers?—what are the take-home points? One set of conclusions refers to the evolution of human fatherhood. Different features of human paternal care, from provisioning to protection to direct care (such as holding an infant), emerged in mosaic fashion, likely during the past two million years. An evolutionary backdrop to derived features of paternal care should also begin with a discussion of the evolution of highly altricial (helpless) and dependent offspring. Early weaning of infants and decreased inter-birth intervals in human evolution necessitated increased investment from a wide range of caregivers—with fathers as central caregivers. Male mating effort in a comparative evolutionary context is also critical to the discussion, as human male involvement in long-term reproductive bonds and paternal care entail shifts toward reduced mating effort and increases in parenting effort. As to the impacts of children on fathers, many of these also align with conceptual shifts in the allocation of male reproductive effort. Male time allocation studies among huntergatherers, for example, quantify features of direct paternal care (e.g., how much and exactly how fathers interact with their children), while such studies in recent large national studies point toward quite modest, if any, changes in men’s work hours when becoming fathers. These kinds of data show that human fathers engage in high rates of direct childcare compared with other apes, and that part of the work fathers do can be viewed as indirect paternal care (i.e., provisioning). The specific allocations of fathers to these and other forms of paternal care vary between and within populations, demonstrating the considerable plas- 136 FATHER DARWIN ticity (rather than determinism) in these investments (Bribiescas et al., 2012). Having children impacts fathers in various other domains. Fathers experience alterations in relationship dynamics, including sexual function. Declines in relationship status are regularly observed in the wake of having a child in Western countries and China, although data on this and other outcomes are lacking from small-scale societies of hunter-gatherers or a wider ethnographic scope. Since most of human sexual behavior is embedded in long-term relationships, a father’s sexual function is often linked with his partner’s (and often child’s mother’s) peripartum shifts in sexual desire and behavior. This period can also heighten sex differences in sexual desire, one area of sexual conflicts of interest, even if a fraction of fathers report decreases in sexual desire. An important consideration to fathers’ experiences is that these are best viewed as part of triadic (mother, father, and child) rather than dyadic (a father-child) phenomena. Children exert psychological, physiological, and health impacts on fathers. As for other aspects of fatherhood, these are best situated in specific social contexts and in light of triadic family (mother, father, and child) dynamics. The emotional impacts of children on fathers can be positive and negative, with a growing literature implicating postpartum depression. The best predictor of male postpartum depression is relationship quality with a child’s mother, in turn invoking the importance of a partnership to paternal experience. Physiological impacts include brain and hormone changes, with declines in testosterone most commonly observed, and typically interpreted within a mating/parenting effort framework. The initial years of involved care of a highly dependent child can yield health tolls on fathers, but some of those health challenges appear to release as the children grow older. While human males appear designed to live shorter lives, on average, than females (consistent with ancestral slight polygyny), involvement in family relationships such as marriage often offers protective effects on male mortality profiles. In that way, male family life can be good for a man’s life. When it comes to providing foundational commentary on the effects of children on fathers, we might recall Darwin’s speculations about the potential positive and negative aspects of marriage—that these could influence men’s fatness, time allocation, and health, among other outcomes. 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