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Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility

Steven W. Gangestad

Reproduction in humans, as in most species, involves sex. For an individual in a sexually reproducing animal species to reproduce, he or she typically must attract a mate, find a mate sufficiently attractive to have sex with him or her, and be adequately compatible genetically with the mate to produce a viable offspring. In many species, including humans, successful propagation of one’s genes through sexual reproduction also requires an investment by one or both parents of time and energy into the well-being of the offspring for at least part of the period from conception to the offspring’s own reproduction. Each of these components of reproduction is a product of evolution and is under selective pressures. Although much about human fertility patterns can be learned in the absence of an evolutionary framework, many details cannot be appreciated except in the light of an understanding of how selection has shaped mating and parenting.

In any specific instance, sexual reproduction is a task that can clearly benefit both the male and the female involved. After all, both individuals’ genes are passed on to an offspring they jointly conceive, and hence the offspring is a vehicle through which each individual’s genes can be propagated. Nonetheless, reproduction should by no means be thought of as a purely cooperative enterprise between mates. Selection will favor individuals’ treating their mates’ outcomes just as important as one’s own when each individual can possibly reproduce only with that particular mate. In such a case, the death of the mate ends the individual’s reproductive career just as surely as does the individual’s own death. By creating living groups of just two individuals—one member of each sex—experimental biologists



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Offspring: Human Fertility Behavior in Biodemographic Perspective 8 Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility Steven W. Gangestad Reproduction in humans, as in most species, involves sex. For an individual in a sexually reproducing animal species to reproduce, he or she typically must attract a mate, find a mate sufficiently attractive to have sex with him or her, and be adequately compatible genetically with the mate to produce a viable offspring. In many species, including humans, successful propagation of one’s genes through sexual reproduction also requires an investment by one or both parents of time and energy into the well-being of the offspring for at least part of the period from conception to the offspring’s own reproduction. Each of these components of reproduction is a product of evolution and is under selective pressures. Although much about human fertility patterns can be learned in the absence of an evolutionary framework, many details cannot be appreciated except in the light of an understanding of how selection has shaped mating and parenting. In any specific instance, sexual reproduction is a task that can clearly benefit both the male and the female involved. After all, both individuals’ genes are passed on to an offspring they jointly conceive, and hence the offspring is a vehicle through which each individual’s genes can be propagated. Nonetheless, reproduction should by no means be thought of as a purely cooperative enterprise between mates. Selection will favor individuals’ treating their mates’ outcomes just as important as one’s own when each individual can possibly reproduce only with that particular mate. In such a case, the death of the mate ends the individual’s reproductive career just as surely as does the individual’s own death. By creating living groups of just two individuals—one member of each sex—experimental biologists

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Offspring: Human Fertility Behavior in Biodemographic Perspective have created these circumstances in laboratory populations. In nearly all natural populations, however, this circumstance rarely if ever exists. Instead, although an ordering of events in terms of the extent to which they would promote or diminish the lifetime reproductive success of an individual may substantially covary with an ordering of events in terms of the extent to which they would promote or diminish the lifetime reproductive success of an individual’s mate, there is rarely perfect covariation. Mismatches in these orderings represent genetic conflicts of interest between the sexes within mateships. These genetic conflicts of interest can produce selection for characteristics of members of one sex that promote the fitness of that sex at the expense of the fitness of the other. The outcome of such selection is referred to as sexually antagonistic adaptation (Rice, 1996). Although sexual conflicts of interest have long been recognized in evolutionary biology, only in the past several years have evolutionary biologists come to appreciate the dramatic ways by which the selection they fuel can influence the dynamics of mating, affect patterns of fertility, and explain outcomes that otherwise appear inexplicable. This chapter paper has several aims. First, I discuss experimental work on the effects of sexual conflicts of interest in laboratory and field populations. Second, I summarize, at a conceptual level, the main consequences of selection fueled by sexual conflicts of interest. Third, I provide an overview of work suggesting that sexual conflicts of interest may have been common in ancestral human populations and hence had opportunity to affect selection on human mating and reproduction. Fourth, I describe three examples of how sexual conflicts of interest have affected specific phenotypic characteristics and mechanisms that, in turn, affect patterns of fertility. Finally, I will discuss the important ways by which sexual conflicts may have varied ancestrally in systematic ways, such that the outcomes of selection fueled by them may be expressed contingently, depending on particular circumstances. EXPERIMENTAL DEMONSTRATIONS OF SEXUAL CONFLICTS OF INTEREST Evolving Male Lines, with No Selection Mediated by Female Success In 1996, William Rice published a spectacular demonstration of sexually antagonistic adaptation fueled by sexual conflicts of interest. Though an ingenious procedure, he allowed Drosophila melanogaster males to evolve while preventing females from evolving counteradaptations. Females in the line were always taken from a nonresponding target stock, whereas males were taken from the adapting-male line. Furthermore, artificial selection procedures ensured that males in the line always passed on the genes

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Offspring: Human Fertility Behavior in Biodemographic Perspective they inherited from their fathers rather than their mothers.). After 30 generations, a series of tests of the relative fitness of males in the experimental line and control males was performed. There was substantial evidence for male adaptation in the experimental line to the target females. Males in the experimental line had increased capacity for remating with females who had previously mated with competitor males taken from the control line. At the same time, competitor males had decreased ability to remate with females previously mated with experimental males and to displace sperm inseminated by experimental males, even when experimental males were not present at the time females were presented with competitor males. In mixed groups the reproductive success of experimental males was 24 percent greater than that of control competitor males. Additional evidence showed that male adaptation evolved at the expense of female fitness. Females that mated with experimental males experienced a death rate greater than that experienced by females mated to control males. No compensating increase in fecundity of females mated to experimental males was observed. Previous research had shown that the protein in male Drosophila melanogaster seminal fluid are a low-level toxin to females (e.g., Fowler and Partridge, 1989; Chapman et al., 1995). Evidence in Rice’s experiment suggested that the mortality cost to females was mediated by both an increase in the remating rate (and hence greater exposure to seminal proteins) and enhanced toxicity of male seminal proteins. The toxicity of male seminal fluids to females is unlikely to be an effect that is itself selected. Rather, evidence suggests that the harmful effect is an incidental by-product of beneficial effects on male reproductive success. The proteins can harm other males’ sperm and hence facilitate sperm competition (Clark et al., 1995; Harshman and Prout, 1994). Furthermore, some seminal proteins appear to enter the female’s circulatory system and thereby influence her neuroendocrine system in ways that benefit the male (e.g., by reducing her remating rate; Aigaki et al., 1991). The costly effects on females are thus to be understood as sexually antagonistic outcomes of male adaptation. Effects of Enforced Monogamy on Sexually Antagonistic Adaptation Wild Drosophila melanogaster typically mate promiscuously, and males make frequent attempts to induce remating on the part of females. Following the dramatic direct demonstration of sexually antagonistic adaptation, Holland and Rice (1999) asked whether enforced monogamy, which relaxes intersexual conflict and increases the benefits of male benevolence toward females, might yield reduced male traits antagonistic to females, thereby reducing a cost of mating to females. They established two replicate

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Offspring: Human Fertility Behavior in Biodemographic Perspective populations. In the control population, a single female was housed with three males (which parallels the sex ratio that takes place during mating episodes in natural populations). In the other population, a single female was housed with a single male. In the latter situation, male reproductive success did not depend on males’ ability to outcompete other males for access to or insemination of a single female. In fact, it depended as much as his mate’s well-being as on his own. Holland and Rice therefore predicted that in the monogamously mated population the seminal fluid proteins would evolve to be less toxic to females, male remating efforts would become less intense, and the net reproductive rate (the number of adult progeny produced per female) would increase.1 All predictions were supported. After 45 generations, test females that had mated once to a male sampled from the monogamous population had greater survival compared to those that mated once to a male sampled from the control population. At the same time, females in the monogamous line died faster than control females when housed with control males. Males in the monogamous line courted females less than those in the control line when housed with females with whom they had evolved. Finally, females in the monogamous line produced a greater number of offspring surviving to adulthood than did control females when females were mated to males with whom they had evolved. Subsequent work has furthermore demonstrated that females mated to males evolved in a monogamous line produce offspring at a higher rate after a single mating than do females mated to control males, purportedly due to the evolution of male benevolence toward females in monogamous lines (Pitnick et al., 2001). Evolution of Female Sexually Antagonistic Adaptations Sexual conflict should be expected to produce female traits that are sexually antagonistic as well as male traits. Hosken et al. (2001) evolved two lines of dung flies: one in which strict genetic monogamy was enforced, the other allowing female polyandry. As expected, males in the polyandrous line had testes of greater size, reflecting the fact that they had evolved to invest greater effort in the production of sperm or other seminal products, which may be involved in sperm competition (see also Pitnick et al., 2001). At the same time, females in this line evolved larger sex accessory glands. These glands produce a spermicidal secretion and thereby influence female ability to affect the paternity of her offspring. Perhaps as a result, 1   As Holland and Rice (1999) note, polyandry could have benefits due to mate choice that outweigh the costs of sexually antagonistic adaptation, and in some species that appears to be the case. Holland and Rice did not observe that outcome in their own experiment, however.

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Offspring: Human Fertility Behavior in Biodemographic Perspective males who mated second with a female from this line had reduced success compared to males mated second with a female from the monogamous line. Sexually Antagonistic Coevolution and Parental Investment Sexual conflicts of interest arise not only in the area of sperm competition and its effects on female well-being but also arise over levels of parental investment. Recently, Royle et al. (2002) demonstrated their effects on parental investment in zebra finches. Male and female pairs of zebra finches typically share parental investment responsibilities of feeding and protecting young. Because rates of adult mortality are appreciable, however, young not uncommonly have a single parent investing in them. Royle et al. were interested in whether the parenting effort of single parents is greater or lesser than that of individuals biparentally investing in offspring. Female birds raised young in two experimental conditions: First, they raised two young to the age of 35 days by themselves; second, the same females raised four young with the father of the offspring to the age of 35 days. The order of these conditions was counterbalanced and controlled. If parents work equally and dedicate as much effort to care in biparental conditions as in uniparental conditions, offspring in the two situations should have fared equally well. If there are nonadditive returns to investment by two parents (e.g., because of greater optimization of own or offspring feeding times owing to sharing of parental duties), offspring in biparental conditions could fare better even if parents exert equal amounts of time and energy to parental duties in the two situations. In fact, however, the opposite pattern was observed: The amount of food consumed per chick when offspring were fed by only the mother was greater than the amount consumed when they were fed by two parents. This difference apparently yielded meaningful fitness effects; as adults, sons raised by single mothers were more attractive to females than were sons raised by two parents. This pattern could occur if fathers typically feed chicks less than mothers do. But comparison of maternal and paternal rates of feeding offspring revealed that fathers provide similar or greater amounts of food to chicks. The likely explanation of these results is that sexual conflicts of interest over rates of feeding result in a net reduction of feeding per chick when two parents share feeding duties. In such circumstances, parents presumably negotiate the extent to which each will feed offspring. Because each parent’s genetic interests are not identical (as neither parent’s future reproductive success is fully dependent on the well-being of the other parent), each parent gains if the other parent takes on a greater proportion of the parental investment in the brood. Modeling of the negotiation game that determines levels of parental investment in situations in which conflicts exist

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Offspring: Human Fertility Behavior in Biodemographic Perspective indicates that it can often result in less investment per parent than the optimal level of parenting by a single parent (McNamara et al., 1999, in press). In effect, each parent may gain by sharply responding to deficits in investment (“free-riding”) by the other parent by their own reductions in effort. (See also Parker et al., 2002.) A CONCEPTUALIZATION OF SEXUALLY ANTAGONISTIC ADAPTATION AND ITS IMPLICATIONS It has long been recognized that species may coevolve with other species in their environments in either a mutualistic or antagonistic fashion. Cases that involve interspecific antagonism are perhaps the more widely recognized and dominate: for example, the coevolution of predator-prey, host-pathogen, or competitors for the same food source. When antagonistic coevolution prevails, new adaptations in one species (e.g., a trait in predators that increases their ability to capture prey) evoke selection on the other species (e.g., on prey) to evolve counteradaptations (e.g., defenses), which may then produce selective pressures on the first species to counter those counteradaptations, and so on. Potentially, antagonistic coevolution of adaptation and counteradaptation can continue through a long period of evolutionary time, resulting in persistent evolutionary change in both species. Antagonistic coevolution is now widely known as the Red Queen process (Van Valen, 1962). This character in Alice in Wonderland claimed that she had to keep running simply to stay in the same place, and so too species must continually evolve to stay competitive against their enemies. Just as genes within two species’ genomes can coevolve in response to their interaction, so too can genes in a single species can coevolve. The more widely recognized and probably dominant case here is mutualistic coevolution. Alleles that “work well” with alleles at other loci are very often selected over alternatives, as illustrated by many commonsense examples. Sonar was more likely to evolve in a flying noctural animal, such as a bat, than in a terrestrial diurnal animal. Penguin wings were more likely to evolve into structures that function much like fins (ineffective for flying) once penguins entered water to feed. Intraspecific genomic coevolution may be antagonistic as well, however. Rice and Holland (1997) refer to such coevolution as interlocus contest evolution, of which sexually antagonistic coevolution is a prime example. Consider, for simplicity’s sake, genes that are sex limited and therefore expressed in only one sex. Genes expressed only in males will be selected for benefits that they provide males. Genes expressed only in females will be selected for benefits that they provide females. Alleles at male sex-limited genes that have negative effects on their male carriers’ mates may nonetheless spread in the population if they benefit males. The evolu-

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Offspring: Human Fertility Behavior in Biodemographic Perspective tion of the adaptations they beget (e.g., seminal proteins that affect female remating), however, set the stage for the evolution of adaptations due to female sex-limited genes that counter those adaptations and their negative effects (e.g., resistance to the effects of the seminal proteins). Such counter-adaptation may then evoke selection for male counters to those counteradaptations (e.g., production of a more intense form or dose of seminal proteins). Ultimately, persistent antagonistic coevolution of male and female sex-limited genes (and the adaptations they beget) in a single species’ genome—that is, an intraspecific Red Queen process—may be the outcome (Rice and Holland, 1997).2 Red Queen processes—including intraspecific ones and hence ones fueled by sexual conflicts of interest—give rise to some predictable evolutionary outcomes. Below, I describe several evolutionary outcomes of sexually antagonistic adaptation that are of note. Relatively Rapid Evolution If, as might be expected, evolution of a new allele at one locus involved in sexually antagonistic selection leads to selection for new alleles at loci that counteract its effects (i.e., are expressed in the other sex), loci involved in sexually antagonistic selection should be characterized by relatively rapid evolution. (Put otherwise, sexually antagonistic adaptations should be less likely to be evolutionarily stable, as they are subject to counteradaptation in the other sex.) As reproductive traits may often be sexually antagonistic adaptations, these traits should and apparently do evolve at rapid rates. For instance, gamete proteins in a variety of species, including mammals, evolve at extremely rapid rates (e.g., Palumbi and Metz, 1991; Vanquier and Lee, 1993; Metz and Palumbi, 1996; Tsaur et al., 2001; Swanson et al., 2001a, 2000b). Furthermore, characteristics of reproductive tracts tend to evolve faster than other traits (and hence, for instance, are more likely to discriminate closely related species than other traits; e.g., Eberhard, 1996). Recent findings show that rapid divergence of reproductive genes has occurred in primates and is marked in the 2   Sex limitation is not required nor necessarily expected of genes evolved through sexually antagonistic coevolution. Perhaps not atypically, genes that benefit one sex in intersexual conflicts actually impose costs when expressed in the other sex (e.g., genes that adaptively increase hormone action in one sex may maladaptively do so in the other sex). These sexually antagonistic genes may be selected if the net benefits to one sex outweigh the costs to the other. Selection should favor modifier genes that limit expression of the gene to the sex benefited by it. Because genes involved in sexually antagonistic adaptations rapidly evolve, however, periods of stable selection on the sex necessary for the evolution of complete sex limitation may not be common. Sexually antagonistic genes compromise the design of each sex away from its optimum. See Chippendale et al. (2001).

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Offspring: Human Fertility Behavior in Biodemographic Perspective divergence of chimpanzees and humans (Wyckoff et al., 2000). This divergence appears to be largely due to positive selection for new alleles (as is expected if antagonistic coevolution is involved) rather than simply relaxation of negative selection against alleles coupled with drift (Wyckoff et al., 2000; see also Swanson et al., 2001a, 2001b). (For theoretical treatments, see also Gavrilets, 2000, and Van Doorn et al., 2001.) Interindividual Variation A corollary of rapid evolution is interindividual variation. In cases of adaptations that represent evolutionarily stable solutions, selection may drive the alleles that map onto the adaptations to near fixation (at least with respect to functionally significant, i.e., nonneutral, variation, the exception being a small proportion of deleterious alleles due to mutation). In the case of sexually antagonistic adaptations, however, rapid evolution may lead to variation being maintained. If selection changes so rapidly that an allele B at locus Z that becomes favored by selection over a predominant alternative allele A at time t1 has not gone to fixation by the time t2, at which a new allele C becomes favored over allele B, then throughout the period during which B was favored (t1 to t2; and, in all likelihood, some period of time thereafter) the population will have always been characterized by variation at locus Z. Even if rapid evolution leads to this situation, only a small-to-moderate proportion of the time, traits affected by multiple loci, each with a nonnegligible probability of being polymorphic at each point in time, may possess significant genetic variation. Fitness traits, including fecundity, typically possess much more genetic variation than ordinary morphological traits and traits known to be understabilizing selection (e.g., Houle, 1992). For instance, whereas human height possesses a coefficient of additive genetic variation (CVA; square root of genetic variation times 100 over trait mean) of about 5, human fecundity appears to possess a CVA greater than 20 (e.g., Burt, 1995; Rodgers et al., 2001). (The same pattern can be observed for traits of Drosophila; Houle, 1992.) Some of the genetic variation in fitness traits can be accounted for by mutation-selection balance (e.g., Charlesworth and Hughes, 1998, who estimate that a CVA of about 8 in Drosophila fitness could be due to mutation-selection balance). Nonetheless, best estimates suggest that not all genetic variation in fitness is owing to mutation. For reproductive traits, coevolution of sexually antagonistic adaptation is a prime candidate to account for a meaningful amount of variation.3 3   Aside from the fact that rapid evolution maintains allelic variation, it may select for a higher rate of mutation and a lack of canalizing processes that modify and narrow the range of gene expression (e.g., Williams and Hurst, 2000). See also note 2.

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Offspring: Human Fertility Behavior in Biodemographic Perspective A Nonnegligible Level of Maladaptation Within Populations It is no wonder that humans have not evolved surefire immunity to pathogen-mediated disease. The pathogens against which we should be selected to defend ourselves are consistently evolving new ways to defeat our defense. Any solution to their attacks is thus likely to be only temporary. Rapid coevolution thus tends not only to produce interindividual variation in adaptation, but the mean level of adaptation to coevolving antagonists in the population will tend to be less than the mean level of adaptation to stable aspects of the environment. Just as this statement should hold true of interspecific coevolution (e.g., host-pathogen coevolution), it should hold true of intraspecific coevolution, such as sexually antagonistic coevolution. Naturally, if individuals vary in the extent to which they possess newly evolving offensive or defensive traits involved in antagonistic coevolution, the load of maladaptation in the population is carried disproportionately by some subset of individuals. Nonetheless, considering the fact that many antagonistic adaptations may be involved, all individuals may be likely to carry some of this load. In the past decade, appreciation of antagonistic coevolution between mothers and the fetuses they carry has led to explanations for why pregnancy appears to be a process that ends in a perhaps surprisingly large proportion of reproductively poor outcomes, in light of the strength of the selection pressures one might expect on reproductive traits. The optimal flow of nutrients from the mother to the fetus from the viewpoint of fetal genes exceeds the optimal flow of nutrients from the viewpoint of maternal genes (Trivers, 1974). Maternal traits and fetal traits may hence antagonistically coevolve as suites of counter-adapted characteristics. Evidence strongly argues for such a coevolutionary process (see Haig, 1993). For instance, human placental lactogen produced under fetal control increases maternal resistance to insulin and thereby acts to maintain longer periods of high blood glucose levels. This effect is countered, however, by increased maternal production of insulin. Haig (1993) has argued that many of the common maladies associated with pregnancy (e.g., hypertension, preeclampsia, gestational diabetes) should be understood as maladaptive by-products of antagonistic coevolution. Reproductive traits involved in mating and conception may also be antagonistic and hence responsible for high levels of maladaptation. The fact that Drosophila melanogaster experience increased reproductive success, even based on single matings, when evolved in monogamous pairs provides indirect evidence for this proposition. Below I discuss one possible area of sexually antagonistic coevolution that may contribute to infertility in humans.

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Offspring: Human Fertility Behavior in Biodemographic Perspective Favorable Outcomes That Depend on the Compatibility of Male and Female Traits There is at least one way in which some intraspecific antagonistic coevolution differs from interspecific antagonistic coevolution. All else equal, an individual of one species (e.g., a predator) experiences reproductive success to the extent that the individual succeeds in the conflict with individuals of antagonistic species (e.g., prey). By contrast, individuals can suffer reproductive costs by dominating too severely a contest with an intraspecific rival. Mothers who are well adapted to restrict transfer of nutrients to a fetus may suffer fitness costs if her fetus is not particularly well suited to obtain nutrients from a resistant mother. A fetus that is well adapted to restrict maternal peripheral blood flow may cause the mother’s death and, ultimately, its own demise if the mother is not well adapted to counter the fetal adaptations. Similarly, male Drosophila with seminal proteins too toxic to his female partner may cause her death prior to her laying fertilized eggs. Females who produce spermicidal secretions that kill sperm of all her mates do not reproduce. Because, on average in the population, genes for antagonistic adaptations may be favored and evolve despite some poor outcomes due to severe overdominance. Compatibilities between male and female features, however, may also affect outcomes. These comparibilities are to be understood as interactions between male and female features on reproductive success. As argued by Zeh and Zeh (2001), compatibility effects caused by sexually antagonistic coevolution may invoke subsequent selection on mate choice to seek mates who possess features compatible with one’s own. Selection for compatible mates appears to be responsible for preferences for mates who possess dissimilar (and thereby compatible) major histocompatibility complex (MHC) genes in mice and rats (for a review, see Penn and Potts, 1999) and perhaps humans (Wedekind et al., 1995; Wedekind and Furi, 1997; but see Jacob et al., 2002; Thornhill et al., in press). This form of compatibility is not obviously one that is the outcome of sexually antagonistic coevolution, however. A recent review by Tregenza and Wedell (2000) noted that several studies show indirect evidence for choice of genetically compatible mates; female choice in some species leads to greater offspring fitness with no clear evidence that their mates provide material benefits or intrinsically good genes. The authors note that there is little evidence for specific sources of genetic compatibility that might drive mate choice for genetic compatibility (the MHC effects being an exception), although they emphasize this area has yet to be well investigated.

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Offspring: Human Fertility Behavior in Biodemographic Perspective THE POTENTIAL FOR SEXUALLY ANTAGONISTIC COEVOLUTION IN HUMANS Thus far I have discussed the general notion of sexually antagonistic coevolution, experimental demonstrations of its effects in populations of laboratory animals, and evolutionary implications of sexually antagonistic selection. The remainder of this chapter examines potential causes and effects of sexually antagonistic coevolution in humans. Human Females: Monogamous or Polyandrous? As noted above, the dramatic reproductive costs of sexually antagonistic coevolution have become widely appreciated in biology only in the past decade. Multiple matings on the part of females (polyandry) increase sexual conflicts of interest and ensuing antagonistic adaptation in the processes that determine conception; female monogamy decreases these conflicts.4 It is ironic, then, that also during the past decade, biologists have come to appreciate the prevalence and level of polyandry, even in species formerly thought to be relatively monogamous. The case of socially monogamous birds is now well documented. On average in these species, the extra-pair paternity rate (percentage of offspring sired by a father other than a female’s social mate, as estimated through DNA fingerprinting) is 10 to 15 percent, with rates of 25 percent or greater not uncommon (Birkhead and Møller, 1995). Zeh and Zeh (2001:1051) have gone so far as to declare an ongoing “paradigm shift” in behavioral ecology, “with the traditional concepts of the choosy, monogamous female and the coadapted gene complex increasingly giving way to the realization that sexual reproduction . . . promotes polyandry . . . .” Whether a true paradigm shift is underway might be debated. Without doubt, however, is the fact that, as the costly outcomes of multiple mating have become appreciated, behavioral ecologists have become all the more aware of the high probability that, at least in many circumstances (including ones in which males provide substantial parental care), polyandry must have substantial benefits to offset these costs and hence is an option that females often pursue strategically. Research on the benefits of polyandry (most notably when it is in the form of extra-pair mating and hence where females have social mates investing in offspring) has identified several possible benefits that fall into two broad categories: material benefits (benefits that directly increase the reproductive success of females) and genetic benefits (benefits that indirectly increase female reproductive success by increasing the viability or 4   As discussed later, multiple matings by both males and females can increase sexual conflicts of interest regarding parental investment.

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Offspring: Human Fertility Behavior in Biodemographic Perspective taining to parenting may influence fertility-related behaviors in a variety of ways. First, they may directly affect child outcomes. Marital conflict is associated with parental parenting strategies, and Margolin et al. (2001) reported evidence consistent with coparenting processes (cooperation and conflict between parents over parental tasks) mediating this association. Marital conflict and conflictual coparenting in turn predict child problem behaviors (e.g., acting out, lack of impulse control; Schoppe et al., 2001), which may be adaptive or maladaptive responses to (from the child’s standpoint) low levels of parental care and guidance. (It should be emphasized that these familial associations may be due to shared genetic influences on behavior rather than direct effects of parenting strategies; unfortunately, no genetically informative study capable of separating these sources of influence has been conducted.) In economically disadvantaged populations in which nutritional stress is common, compromises to parental care owing to sexual conflicts of interest may affect the growth and developmental health of children. Second, these conflicts may influence processes that affect the interbirth interval (as well as, in certain circumstances completed family size). One might expect that heightened conflict between spouses over child care duties may delay willingness on the part of one or both partners to have another child or, in natural fertility populations, increase the interbirth interval by, for instance, increasing the age at weaning. Third, anticipation of conflicts of interest may influence desires to have children with a current partner and hence motivation to start a family. Although research has extensively documented heightened conflict between new parents, we know very little about the nature of the tactics that partners use in attempts to enhance participation in parenting by the other parent or countertactics to subvert these attempts. Similarly, we know very little about the costs of these tactics to parenting and thereby children. We should expect that these tactics revolve more around controlling how the male partner allocates his time and effort than around how the female partner does so. Because women may withdraw parental investment to enhance male participation, however, conflicts over female parenting may also arise. Furthermore, although the initial arena of conflict may concern parental efforts, influence tactics may spread to other aspects of the relationship, as partners reinforce parenting efforts (or punish lack of such efforts) by introducing contingencies on other valued behaviors (e.g., if the male partner prefers a higher rate of sexual behavior, females may initiate or respond to male attempts to initiate sex contingent on male parenting efforts). As noted earlier, the optimal allocation of male effort to parenting should (or ancestrally should have) depended on payoffs to parenting as well as payoffs to other activities (e.g., those related to seeking additional mating opportunities). Because work on the transition to parenthood has

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Offspring: Human Fertility Behavior in Biodemographic Perspective not been informed by an evolutionary perspective on sexual conflicts of interest (but rather has tended to view this transition as a normal period of “adjustment” that parents undergo), research has not systematically examined the impact of factors that moderate these payoffs on conflicts. Males who possess characteristics that make them more attractive to females in general may be more reluctant to engage in parenting efforts (for an avian example, see Smith, 1995). If so, do they experience more conflict with their partners over parenting? Or, just as females in a number of bird species increase parenting efforts with more attractive males (for a review, see Sheldon, 2000), might the negotiation process lead to greater allocation of effort on the part of their partners (see Boussière, 2002, on cost-benefit modeling)? Because men with partners who would be difficult to replace may perceive greater costs to efforts to seek other mating opportunities, female features (e.g., attractiveness) should also affect the degree of and resolution of conflict over parenting. Finally, conflict may also depend on characteristics of the child. The perceived marginal gain as a function of parenting may differ for children of different developmental qualities or health. For these offspring, then, fewer benefits from other activities are necessary for those activities to compete with parenting effort, and conflict over their care may be greater. These possibilities may be explored in future research. Just as coevolutionary processes may be responsible for variation in men’s and women’s control over immunologic activity in the female reproductive tract, they may have created differences in men’s and women’s influence over the negotiation process regarding parenting. And just as matching of men’s and women’s abilities to control immunologic activity may affect fertility outcomes, matching of men’s and women’s influence over the negotiation process may importantly affect parenting and thereby child outcomes. FACULTATIVE EXPRESSION OF SEXUALLY ANTAGONISTIC ADAPTATIONS IN HUMANS? Sexually antagonistic coevolution is fueled by differences in the genetic interests of male and female mates in the absence of strict genetic monogamy. When strict or relative monogamy reigns, whether in natural or laboratory populations, males and females should evolve relative benevolence toward mates. As mating departs from monogamy, conflicts increase, selection for sexually antagonistic traits is strengthened, and a reproductive load on mortality or fecundity should result (Holland and Rice, 1999). Women show evidence of design for strategic polyandry. Furthermore, at least one modern human population is characterized by a rate of extra-

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Offspring: Human Fertility Behavior in Biodemographic Perspective pair paternity that would fuel considerable sexual conflicts of interest. Not unlikely, many ancestral human groups were exposed to similar levels of sexual conflict. At the same time, at least one modern population is characterized by a very low rate of extra-pair paternity, and, not unlikely, some ancestral human groups were similarly exposed to low levels of sexual conflict. Quite possibly, humans have evolved patterns of mating and parental investment that are variable in nature and contingently expressed as a function of ecological and/or socioecological factors. (See Gross, 1996, for a discussion of conditional mating strategies.) In part, the contingent expression of reproductive tactics should be a function of factors that affect the benefits and costs of polyandry, which may include, but not be limited to, (a) the degree to which men vary with regard to intrinsic genetic benefits (e.g., the prevalence of parasites or environmental stress, both of which may potentiate expression of fitness-relevant genetic variation; Gangestad and Simpson, 2000) and (b) the degree to which paternal investment adds to offspring fitness, possibly as a function of the extent to which maternal and paternal investment multiplicatively influence offspring fitness (e.g., through division of labor; Kaplan et al., 2000). Just as mating and parenting tactics in general may have evolved to be facultatively expressed, so too sexually antagonistic tactics may have evolved to be contingent responses in men’s and women’s reproductive strategies. Hence, just as male Drosophila evolve to be more benevolent toward their mates when strict monogamy is enforced, men and women may be more benevolent when conditions favor relative monogamy. By contrast, just as male Drosophila impose a reproductive load on females when mating is promiscuous, men and women may express adaptations that impose reproductive costs on the other sex when conditions favor multiple matings. With regard to the three illustrations sketched above, one might expect that (a) the expression of imprinter genes may be adaptively contingent on environmental factors, such that imprinting, maternal-fetal conflict, and the reproductive load (e.g., fetal insufficiency, maternal stress) that results increase as a function of factors favoring polyandry and ease as a function of factors favoring relative monogamy (see Haig, 1993, and Trivers and Burt, 1999, for related remarks); (b) the struggle over control of immune function in the reproductive tract and its reproductive load (e.g., infertility, spread of STDs) are enhanced by factors favoring polyandry and eased as a function of factors favoring relative monogamy; (c) conflicts between parents will be reduced, care and provisioning will be more efficiently and effectively provided to offspring, and offspring health and features of adaptive functioning affected by parental care will be enhanced under circumstances in which men are motivated to engage in parental care rather than seek multiple mating opportunities.

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Offspring: Human Fertility Behavior in Biodemographic Perspective SUMMARY Sexual mates have correlated interests in favorable reproductive outcomes. Because their interests do not perfectly correspond, however, sexual conflicts of interest also exist. These conflicts can lead to sexually antagonistic coevolution, in which each sex evolves adaptations that benefit mates of that sex at the expense of the interests of mates of the other sex. This coevolution process typically results in a reproductive load on the species, reducing the efficiency by which sexual pairs produce and care for offspring. An understanding of fertility-related behavior and processes can be informed by an appreciation of how sexual conflicts of interest have manifested in sexually antagonistic features. Only under conditions of true genetic monogamy (in which each sex can potentially reproduce with one mate only) do sexual conflicts of interest fail to exist. Multiple matings by members of both sexes (whether serially or simultaneously) create sexual conflicts of interest. In species in which females are inseminated, polyandry fuels sexual conflicts of interest over control of paternity. In these species in which both sexes invest in offspring, polygyny fuels sexual conflicts of interest over coparenting efforts. Polyandry and polygyny both contribute to sexual conflicts of interest over the flow of resources from mothers to offspring. Evidence for adaptations that result from each of these conflicts of interest in a variety of nonhuman species are well documented. Adaptations underlying human fertility-related behavior and processes that may have been shaped by sexually antagonistic coevolution are an area ripe for exploration. REFERENCES Aigaki, T., I. Fleischmann, P.S. Chen, and E. Kubli 1991 Ectopic expression of sex peptide alters reproductive behavior of female Drosophila melanogaster. Neuron 7:557-563. Baker, R.R., and M.A. Bellis 1995 Human Sperm Competition: Copulation, Masturbation, and Infidelity. London: Chapman and Hall. Bellis, M.A., and R.R. Baker 1990 Do females promote sperm competition? Data for humans. Animal Behavior 40:997-999. Belsky, J., and K.H. Hsieh 1998 Patterns of marital change during the early childhood years: Parent personality, coparenting, and division-of-labor correlates. Journal of Family Psychology 12:511-528. Birkhead, T.R., and A.P. Møller 1995 Extra-pair copulation and extra-pair paternity in birds. Animal Behavior 49:843-848.

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