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Offspring: Human Fertility Behavior in Biodemographic Perspective (2003)

Chapter: 8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility

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Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
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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

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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-

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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).

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×
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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×
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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

mating success of offspring). Traditionally, material benefits have been more widely accepted: for instance, direct nutritional benefits, physical protection, confusion of paternity (see Zeh and Zeh, 2001). In recent years, however, genetic benefits have garnered considerable support (for a review, see Jennions and Petrie, 2000). These benefits fall into three main categories: (1) intrinsic good genes: choice of an extra-pair mate who has genes that additively enhance offspring fitness independently of maternal genes (e.g., lack of mutations, favorable disease resistance genes involved in antagonistic interaction with pathogens, favorable genes involved in sexually antagonistic interaction, as discussed in this paper); (2) compatible genes: choice of an extra-pair mate who has genes that are compatible with female genes (with compatibility possibly the outcome of sexually antagonistic coevolution) and thereby enhance offspring fitness; (3) diverse genes: choice of an extra-pair mate whose genes will diversify the genetic makeup of the female’s offspring, which may have any number of benefits (e.g., a hedge against environmental uncertainty, reduced chances of an intrafamilial disease epidemic). (For more fine-grained discriminations, see Jennions and Petrie, 2000; Zeh and Zeh, 2001.) It is beyond this chapter to review the relative strength of evidence for these benefits. It should be noted, however, that the benefits of polyandry need not be mutually exclusive; within single species, multiple benefits may account for extra-pair mating.

Published studies that have estimated the extra-pair paternity rate in human populations based on DNA or serological data are scant. Only two full reports exist. One estimated a rate of less than 1 percent in a Swiss population (Sasse et al., 1994). The other estimated a rate of 11 percent in a population from Monterrey, Mexico (Cerda-Flores et al., 1999). In the latter study, the extra-pair paternity rate varied as a function of socioeconomic status. Whereas it was about 5 percent in the high socioeconomic status population, it was estimated to be 20 percent in the low socioeconomic status population. Obviously, generalizations from data on only two populations are risky. They do suggest, nonetheless, that (1) the extra-pair paternity rate can be very substantial in human populations and (2) its range across populations is very considerable. One possibility is that ecological and socioecological circumstances that moderate the benefits of polyandry account for the variability through expression of environmentally contingent mating and parenting strategies of humans, a possibility explored in greater detail in a later section.

Another Source of Evidence for Polyandrous Tendencies: Design for Polyandry

Sexually antagonistic coevolution of adaptations in modern humans would have occurred in ancestral populations. A tack for addressing whether ancestral females engaged in polyandry as a strategic option is to

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

look for evidence that women possess features apparently designed for obtaining benefits through polyandry. Several years ago, Randy Thornhill and I proposed to look for a set of features in women that may have design for obtaining genetic benefits from extra-pair men (Gangestad and Thornhill, 1998). Specifically, we proposed that, if ancestral women could have obtained genetic benefits through extra-pair sex but at some risk of cost (perhaps largely due to loss of a mate’s parental investment in her offspring), selection may have forged preferences for phenotypic indicators of those genetic benefits to be conditional and depend on women’s phase of the menstrual cycle: be most pronounced during the fertile phase of the cycle, when such benefits could be garnered, and subdued outside the fertile phase. As Penton-Voak et al. (1999) added, this shift should be most notable in women’s preferences for a sex partner (or “short-term” partner) and perhaps absent in women’s preferences for a long-term mate. The straightforward evolutionary economic reasoning is that, if there are no benefits to be gained, there is no sense in paying costs. Benefits can only possibly exceed costs when the possibility that they can be garnered is nonzero.

We and others have largely applied this reasoning to look for a design for obtaining intrinsically good genes, though more recently we have looked for a design for obtaining MHC-compatible genes. Several preference shifts across the cycle have now been demonstrated and in some instances replicated multiple times:

  1. Preference for the scent of symmetry. Fluctuating asymmetry (FA) is lack of symmetry on bilateral traits that are symmetrical at the population level and is thought to be the outcome of developmental instability, errors in development due to perturbations such as mutations, pathogens, and toxins (for a review, see Møller and Swaddle, 1997). It appears to be partly heritable (Gangestad and Thornhill, 1999, in press-b; but see also Fuller and Houle, in press). We measure 10 such traits in humans and sum the standardized asymmetries to form a single index of FA as a measure of developmental instability. Our studies show that men who possess low FA tend to have greater numbers of sex partners (Gangestad et al., 2001, 2002b; Gangestad and Thornhill, 1997a; Thornhill and Gangestad, 1994), an effect that appears to be partly mediated by phenotypic traits such as social status and intrasexual competitiveness (e.g., Gangestad and Thornhill, 1997b; Simpson et al., 1999). In three studies we have found that normally ovulating women (those not using hormone-based contraception) prefer the scent of symmetrical men, though only when in the fertile phase of the cycle (Gangestad and Thornhill, 1998; Thornhill et al., 2002; Thornhill and Gangestad, 1999). The correlation between preference for the scent of symmetrical men and fertility risk estimated from the day of the cycle and actuarial data when all samples are aggregated is .40. The regression-based

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

estimated preference when fertility is zero is close to nil. This effect has been replicated in a fourth study performed in Vienna (Rikowski and Grammer, 1999).

  1. Preference for male facial masculinity. By manipulating digital images, Penton-Voak et al. (1999) created male faces varying with respect to masculinity and femininity. Three studies (two in the United Kingdom, one in Japan) have shown that the face women find most attractive just prior to ovulation is more masculine than the one they most prefer outside the fertile phase (Penton-Voak et al., 1999; Penton-Voak and Perrett, 2000). Using a somewhat different methodology, Johnston et al. (2001) replicated this effect in the United States and, importantly, found that women’s ratings of female facial attractiveness was not affected by menstrual phase. Penton-Voak et al. explicitly asked women to rate men’s attractiveness as a short-term mate (i.e., a sex partner) and a long-term mate. Fertility risk interacted with relationship context to affect preferences. Greater preference for masculinity just prior to ovulation was observed only when women were rating attractiveness as a short-term mate. Men’s facial masculinity covaries with their body symmetry (Gangestad and Thornhill, in press-a), and hence shifts in preference for facial masculinity and the scent in symmetry are shifts in preference for correlated indicators.

  2. Preference for men’s behavioral displays. Gangestad et al. (2002a) had women view brief videotaped segments of men interviewed for a potential lunch date by an attractive female and rate the attractiveness of each man as a sex partner and long-term mate. A large number of nonverbal and verbal features of the interviews were coded, and, through principal components analysis, two major dimensions discriminating men’s performance were identified: social presence (e.g., direct eye contact, lack of downward gaze, confidence) and direct intrasexual competitiveness (e.g., derogation of a competitor male, direct comparisons of self with the competitor). A fertility risk by relationship context interaction effect on preferences for these two sorts of displays was found, one paralleling that reported by Penton-Voak et al. When at high fertility risk, women particularly preferred men who evidenced social presence and direct intrasexual competitiveness as short-term mates. Fertility risk did not influence preference for the displays in long-term mates. Based on these same interviews, Simpson et al. (1999) reported that men’s direct intrasexual competitiveness covaries with their symmetry, and, thus once again, these preference shifts concern features that at least partly overlap with other features for which preferences shift.5

5  

In an effort to test whether women might also seek compatible genes at midcycle, Thornhill et al. (2002) examined menstrual cycle effects on women’s scent preference for MHC dissimilarity. They found no evidence for shifts across the cycle and, in fact, did not replicate previous findings that women prefer the scent of individuals dissimilar at MHC (Wedekind et al. 1995; Wedekind and Furi, 1997). See also Jacob et al. (2002).

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

Gangestad et al. (2002b) asked women how often in the past 2 days they had experienced sexual attraction to or fantasized about men other than a primary partner as well as their primary partners twice during the cycle: once within 4 days before or a day after a lutenizing hormone surge (i.e., at high fertility risk) and once in the mid-to-late luteal phase. As might be expected, if women found a suite of features particularly sexy (attractive in a short-term partner) just prior to ovulation, they reported greater sexual interest in men other than primary partners just prior to ovulation. No comparable shift in women’s interest in their own partners was detected. Naturally, these shifts in sexual interest may only occasionally lead women to have extra-pair sex. Nonetheless, when they do, they might well be more likely to do so midcycle. Bellis and Baker (1990) surveyed British women and found precisely that pattern. By contrast, women’s sex with their primary partners was more evenly distributed across the cycle.6

These studies suggest that, like females of many other species, polyandry may have been part of the tactical repertoire in the reproductive strategy of ancestral females (albeit one whose expression evolved to be conditional on environmental circumstances). Although to evolve as a reproductive tactic, female polyandry must have had benefits, it also had costs. Many of those costs should be understood as the outcomes of sexually antagonistic coevolution.

A premise of the expectation that female interest in markers of genetic benefits in sex partners should be contingent on female fertility risk was that females could pay costs by engaging in extra-pair sex, largely because their male partners will be less willing to invest in their partners’ offspring if they know or suspect that their partners have engaged in extra-pair sex. The decision process that underlies male willingness to invest in offspring can itself be thought of as a coevolved counteradaptation to female polyandry. In fact, the same study that found that female interest in extra-pair men is contingent on female cycle phase found evidence that male counteradaptation to female polyandry is similarly honed by selection to be sensitive to the female cycle phase. Women were asked the extent to which their primary partners had, in the past 2 days, engaged in a number of “mate retention tactics,” such as vigilance (frequent checking up on them) and monopolization of their time. Women reported that their partners had been both more proprietary (e.g., vigilant) and attentive (e.g., monopolizing of time) during the high-fertility days prior to ovulation than during the luteal phase (Gangestad et al., 2002b). Although men could be interested in spend-

6  

The sample in this study was highly self-selected, as female readers of Parade magazine were asked to respond to a survey. It is unclear how the nonrepresentative nature of the sample would generate the observed interaction between relationship type (extra-pair vs. in-pair) and menstrual phase. Nonetheless, the findings bear replication.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

ing time with their partners for any number of reasons, interestingly the men most likely to have increased interest in doing so midcycle tended to be those with partners who expressed increased sexual interest in extra-pair men—not their primary partners—during this same period. The pattern of findings suggests that either (a) men have evolved to respond to whatever residual cues of fertility status (e.g., scent; Singh and Bronstad, 2001) exist by engaging in greater mate guarding when the costs of their partners’ extra-pair sex are greatest, particularly when cues suggest risk that their partners may have extra-pair sex at that time, or (b) men have evolved to the cues that their partners have increased interest in extra-pair men themselves. In either case, the outcome should be understood as a counteradaptation to polyandry.

The Effects of Polygyny on Sexual Conflicts of Interest

Female multiple matings create sexual conflicts of interest in the area of fertilization processes. Whereas an individual male benefits from having his own sperm father a female’s offspring, the female’s interests may be best served by having another sire for her offspring. Polygyny (male multiple matings) in the absence of polyandry can also create conflicts of interest. For instance, males may benefit from rates or lengths of mating bouts different from those that would optimize female fertility. These effects on sexually antagonistic coevolution, however, are probably small in comparison to the effects of female multiple matings. Female multiple matings create conflicts over paternity, in which case whether a male reproduces at all is at stake. It is unlikely that male multiple matings can impact female reproductive success as dramatically.

When males invest in offspring, however, male multiple matings can foster conflicts of interest over parental care. From the male’s point of view, there is some optimal mixture of effort dedicated to parenting and effort to seek additional mates. This mixture deviates from the optimal allocation of male effort from the female’s point of view, which includes no effort dedicated to seeking additional mates. Conflict hence arises over the allocation of effort that males exert on parenting and, conversely, efforts to seek other mates. As noted above, when conflicts of interest over parenting effort exist, the negotiation process can lead to lower allocations of parenting effort than single parents would expend.

Human males have probably evolved to invest considerable amounts of time and effort toward enhancing the well-being and productive development of offspring (e.g., Kaplan et al., 2000), albeit contingently based on a variety of factors (e.g., Geary, 2000). Naturally, male parental effort would not have evolved had it not had a considerable impact on offspring quality or the rate at which female mates could reproduce. At the same time,

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

however, men probably also evolved to seek additional mating opportunities, albeit also conditionally (e.g., dependent on his success in attracting additional mates; Buss and Schmitt, 1993; Gangestad and Simpson, 2000; Trivers, 1972). Indeed, if, as argued above, ancestral women sometimes benefited from extra-pair matings with men who did not invest in resulting offspring, it stands to reason that men would have evolved to seek and compete for those mating opportunities. Studies of human sexual interest reliably find that men’s interest in sexual variety and multiple matings exceeds that of women. One study, for instance, found that, on average, college men reported that they would optimally have 10 sexual partners in the next 3 years (Buss and Schmitt, 1993; see also Schmitt et al., 2001). By contrast, women reported that they would optimally have, on average, two partners over the same time period. As men’s efforts to seek additional mates would not have increased their primary mates’ reproductive success, male-female conflicts of interest over men’s efforts to seek multiple mates should have existed. These conflicts should have resulted in the evolution of sexually antagonistic adaptations used in the negotiation of parenting effort.7

As discussed earlier, outcomes of sexually antagonistic adaptation in one sex may have clear fitness costs for the other sex, either in the form of reduced viability or reduced fecundity. The next section discusses three examples of antagonistic adaptation with such costs that may have evolved in humans.

ILLUSTRATIONS OF ADAPTATION AND COUNTER-ADAPTATION IN HUMAN SEXUALLY ANTAGONISTIC COEVOLUTION

Potentially, many human features have evolved through sexually antagonistic coevolution. Every tactic of persuasion that, if successful, increases the persuader’s reproductive success at the expense of the reproductive success of the target of persuasion should eventually be met by evolved resistance to the persuasion. Across the animal world, courtship rituals may be packed with such counter-adapted complexes. Undoubtedly, some advertisements in the biological world (such as the peacock’s tail; Petrie, 1994) are honest indicators of underlying quality that members of the other

7  

Because female multiple matings could potentially take away from parenting effort, it stands to reason that multiple matings may also have fueled some conflict over parenting. Because females should not be expected to have to pay the same heavy costs in mating effort that men do (because men should be motivated to seek opportunistic matings with women), however, the effect of female multiple mating on the negotiation of allocation of effort to parenting (independent of its effects on paternity) should be small relative to the effect of male multiple matings. When females do engage in mating effort at the expense of parenting, however, it should naturally be a source of conflict between mates.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

sex benefit from valuing. Nonetheless, each sex may have sensory biases that favor certain displays that offer no quality of true value to the chooser. Selection should lead choosers to resist being influenced by these advertisements. Ironically, however, one possible outcome of one sex’s resistance to the other sex’s displays is evolved exaggeration of the display (see Holland and Rice, 1998, on “chase-away sexual selection”; but see also Getty, 1999, and Rice and Holland, 1999). It seems likely that the human courtship repertoire possesses coevolved elements of false advertisement and resistance, but this issue has hardly been explored. Another potential area of conflict in the domain of fertility-related behavior is the frequency and timing of intercourse. When the probability of female multiple matings is nonzero, the optimal rate and timing of intercourse for male and female members of a pair may differ (with males preferring a higher rate).

Three particular potential sets of adaptations that evolved through sexually antagonistic coevolution are discussed below. The first two concern processes directly involved in the mechanics of reproduction: pregnancy and conception. I have chosen them as illustrations because (1) they involve physiological mechanisms that have been observed or are, in principle, directly observable; (2) they are directly involved in reproduction; (3) at least potentially they have fertility (and possibly other) costs that, by all reasonable inference, are part of the reproductive load imposed by sexual conflicts of interest; and (4) although a variety of predictions can be derived from well-reasoned theory, most of these predictions have not yet been assessed, and hence these examples illustrate how theory about sexually antagonistic coevolution can guide future research. The last illustration concerns parenting efforts, a realm that may importantly affect fertility outcomes in humans.

Genomic Imprinting

Genomic imprinting refers to differential expression of genes depending on the parent of origin. In the instance of nonimprinted genes, both the paternally derived and maternally derived alleles are active. In the case of imprinted genes (of which there appear to be approximately 100 in mammals; Mochizuki et al., 1996), either the paternal or the maternal copy of the gene is more active than the other. In many cases the less active allele is completely silent. The evolutionary theory of imprinting that is most accepted to date, both because of its logical coherence and empirical support for it, is Haig’s kinship theory (for a recent review, see Haig, 2000). This theory states that imprinting evolved because of conflicts of interest of offspring genes with maternal genes that differ depending on whether they are derived from the mother or the father. Although this conflict may arise in a number of different contexts (see Trivers and Burt, 1999), the most

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

clearly supported is in the fetal-maternal conflict over parental investment in the offspring. Maternally derived genes will occur in the mother’s future offspring 50 percent of the time. In the absence of strict genetic monogamy, paternally derived alleles will occur in the mother’s future offspring less than 50 percent of the time. (In the extreme case in which mothers and fathers produce at most one offspring together, this value is 0 percent. As noted by Parker et al., 2002, however, even when mothers are sexually monogamous, sexual conflicts can exist because males can potentially mate with other females, and hence their future reproduction need not depend on the well-being of a single female.) It follows that genes that affect the growth of a fetus and hence its nutritional demands on the mother are strong candidates to be imprinted, with growth promoters expected to be active when paternally derived and growth suppressors expected to be active when maternally derived. In fact, a host of imprinted genes in both humans and mice follow this pattern.8

Imprinting (the silencing of gene expression) requires special machinery, which begins in the production of male and female gametes. At least in many cases it involves methylation of DNA (e.g., REF). DNA methylation of alleles in the production of gametes requires the action of a gene that applies this imprint (or genes that do so), which may be cis-acting or trans-acting (on the same chromosome or a different chromosome, respectively). For genes to differentially apply imprints to maternally or paternally derived copies, they must be differentially expressed in the male and female, that is sex limited in their expression. Hence, the evolution of imprinting involves sexually antagonistic coevolution of male and female imprinter genes (see Zeh and Zeh, 2001). Paternal imprinters can be construed as adaptations that increase the viability of the fetus at the cost of the mother’s viability. Evolution of these adaptations sets the stage for counteradaptation involving maternal imprinting.9

We should expect that, like other antagonistic coevolutionary processes, the coevolution of imprinting should yield the evolutionary outcomes discussed earlier.

8  

Genes on the Y chromosome, like paternally imprinted genes, are expressed only as paternal copies. As expected, the genes that favor fetal growth tend to accumulate on Y. The Y thus is expected to accumulate genes that enhance fetal demands on maternal resources. Moreover, in instances in which a mother’s offspring do often have the same father, Y genes will be selected to favor subsequent brothers at the expense of sisters because brothers share Y, whereas sisters do not. Maternally active genes on X may evolve to counteract selfish growth factors on Y, and paternally active X genes (passed on only to daughters) may evolve to favor sisters. For details and other complications with sex chromosomes, see Trivers and Burt (1999), Haig (2000), and Hurst (1994).

9  

One interesting complication not dealt with here is that imprinter genes can be in conflict with the genes they imprint. See Burt and Trivers (2000).

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×
  1. Imprinter and/or imprinted genes should evolve rapidly. Although some analyses suggest that imprinted genes are characterized by frequent positive selection for functional DNA substitutions, the evidence to date is not compelling (Trivers and Burt, 1999). Little is known about the rate of evolution of imprinter genes.

  2. Imprinter and/or imprinted genes should be characterized as substantial allelic variation. Little appears to be known about the polymorphism of imprinter genes. A recent study examined expressed polymorphisms in blood for three imprinted human genes, IGF2 (insulin-like growth factor II), SNRPN (nuclear ribonucleoprotein N), and IMPT1 (multimembrane-spanning polyspecific transporter-like gene 1) in a normal Japanese sample (Sakitani et al., 2001). The first two genes are paternally active, while the latter is maternally active. Consistently, only the paternal copy of SNRPN was expressed. By contrast, notable variation in the expression of the maternal copy of IGF2 was observed, and there was very substantial variation in the degree to which the paternal copy of IMPT1 was expressed. It is not known at this time whether the individual variation in expression of these imprinter genes is due to allelic variation in imprinter genes, though that is one possibility.

    Of the many genes whose allelic variation has been examined in relation to IQ, the only one whose association has been multiply replicated is IGF2R (insulin-like growth factor 2 receptor), a maternally active imprinted gene (Chorney et al., 1998). One possibility is that the current variation we observe is but a snapshot in an evolutionary scenario in which one allele is replacing another through positive Darwinian selection driven by sexually antagonistic genetic interests. This possibility has not been evaluated.

  3. The antagonistic coevolution of interests of maternally and paternally derived fetal genes (and the sex-limited imprinter genes that account for imprinting) should be a source of maladaptation. As discussed earlier, antagonistic adaptations that evolved in response to the maternal-fetal conflict appear to be responsible for a variety of poor reproductive outcomes of pregnancy. One should expect that some of the fetal adaptations antagonistic to maternal well-being are paternally active imprinted genes. The genetic bases of many of these adaptations (e.g., manipulation of hormone levels in the maternal bloodstream, partly responsible for gestational diabetes and hypertension) is unknown.

  4. Favorable outcomes should partly be a function of compatibility between maternal and paternal imprints. Imprinted genes evolve in a context in which only one copy of the gene is (typically) expressed. Paternally active alleles should be selected to be strongly expressed when maternal copies are silenced. But the optimal situation from the standpoint of the paternally derived genes is not unfettered expression. In principle, the fetus

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

may grow at a rate far greater than optimal even from the perspective of paternally derived genes, for the result may be spontaneous abortion or death of the mother (see Haig, 1993). Similarly, the fetus may demand resources at a level far less than is optimal from the standpoint of growth-suppressing maternally imprinted genes, for the fetus may be deprived. Fetuses differing in their relative expression of paternally active imprinted genes may optimally thrive when paired with different maternally active imprinted genes. On average, for instance, the success of strongly expressed paternally active genes may be maximized when paired with maternally active imprinted genes that are expressed more strongly than those that would maximize the success of more weakly expressed paternally active genes (Zeh and Zeh, 2001). Mismatches in expression of imprinted genes are expected to account for a meaningful proportion of poor pregnancy outcomes.

Conflict Over Immunosuppression in the Female Reproductive Tract

As discussed earlier, proteins in male Drosophila seminal fluid are low-level toxins to females, effects that are at least partly by-products of selection for ability to effectively engage in competition against other males’ sperm. In addition, some seminal fluid proteins in Drosophila are absorbed into the female bloodstream, mimic her hormones, and thereby manipulate her responses. Human seminal fluid also carries a host of products (e.g., proteins, fatty acids) with sperm into the female reproductive tract. As far as is known, these products do not have directly toxic effects on females. Moreover, there is no compelling evidence that components of human seminal fluid play a major role in sperm competition (cf. Baker and Bellis, 1995). Seminal products presumably have evolved functions, however, and it should not be surprising if some of these functions have been selected through sexually antagonistic coevolution, with deleterious effects on female viability and/or fecundity.10

Vaginal, cervical, and uterine mucosa are rich in immunological factors, including leucocytes, cytokines, immunoglobulins, and antimicrobial peptides (e.g., Quayle et al., 1998; Yeaman et al., 1998). A primary function of their presence is likely as a defense against sexually transmitted diseases (STDs). Indeed, a recent comparative analysis of primates found that, controlling for group size and exposure to soilborne pathogens, white

10  

Mimicry of female hormones and manipulation of responses should not be discounted as a possibility; after all, prostaglandins are primarily female hormones in humans and importantly function during pregnancy, with large concentrations in men found only in the prostate, where they are manufactured for release into seminal fluid.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

blood cell counts are greater in species in which females have more mating partners and hence species in which STDs are a greater risk, suggesting that STDs have been a significant selective pressure on the evolution of primate immune systems (Nunn et al., 2000). Cell-mediated and humoral immune responses in the reproductive tract, however, may attack not only pathogens but also sperm subject to attack or trapping (e.g., Hirano et al., 1999). Female immune responses can, in principle, eliminate the possibility of successful fertilization and indeed appear to play a role in some instances of infertility (e.g., Harrison et al., 1998; Mazumdar and Levine, 1998; Hirano et al., 1999). Immunological defense in the reproductive tract, then, has both benefits and costs, and presumably there is some optimal trade-off maximizing net benefit.

From the male perspective, these same costs and benefits may also operate, particularly when there is some probability of having subsequent offspring with his female mate. Nonetheless, because (1) in the absence of strict monogamy, his future reproductive success need not be tied to hers, (2) immunological factors in the female reproductive tract probably function to prevent male-to-female transmission of STDs more so than female-to-male transmission; (3) there may be greater reproductive costs of STDs to females than males (due to greater association with sterility [Westrom, 1994], possibly an effect that evolved to benefit sexually transmitted pathogens), it seems likely that the level of immunological capacity in the female reproductive tract maximizing male reproductive success is less than what is optimal from the female point of view. In all likelihood, there is a sexual conflict of interest in this area.

In recent years, medical research has shown that a variety of products in human male seminal plasma have immunosuppressive effects. For instance, prostaglandins, which are major constituents of seminal plasma, stimulate the production of the antiinflammatory cytokine interleukin-10 (IL-10; Kelly et al., 1997; Denison et al., 1999) and inhibit the production of the proinflammatory cytokine IL-12 (Kelly et al., 1997). IL-10 inhibits the killing activity of T-cells and natural killer cells and thereby suppresses cell-mediated immune responses, whereas IL-12 promotes cell-mediated immunity. Jeremias et al. (1998) similarly reported that human semen produces messenger RNA for IL-10 in female blood cells and, furthermore, can inhibit production of IFN-g, a proinflammatory cytokine. Some effects appear contrary to the general trend (e.g., prostaglandins may also enhance production of IL-8, a proinflammatory cytokine; Denison et al., 1999); possibly, the overall effect is more complexly patterned than simply a general immunosuppressive effect. (For instance, it may be that the capacity to attack viruses and foreign antigens in particular is suppressed, with attacks triggered by bacterial chemical trails unchanged or enhanced.) At present, however, it does seem clear that at least some components of seminal

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

plasma function to suppress both cell-mediated and humoral immune responses (Kelly, 1997).

Immunosuppressive functions make perfect sense when viewed through the lens of sexually antagonistic coevolution. Indeed, if there exists a sexual conflict of interest over the capacity for immunological responses in the female reproductive tract, one should expect males to have evolved to suppress these immune functions, females to have countered by increasing allocation of effort to them, males to have responded by increasing immunosuppressive efforts, and so on, in an escalating coevolutionary tug-of-war. Evidence for such a tug-of-war could be that females counteract male immunosuppressive activity by, for instance, disabling those functions. Alternatively, females may have undermined attempts to suppress immune function by evolving immunostimulators that are enhanced by the same male products evolved to suppress activity. (Indeed, one possible explanation for certain immunostimulatory effects of male seminal plasma is precisely this counteradaptation; future research may address this possibility.) At the present time, there is neither evidence strongly in favor or against antagonistic coevolution, as it appears that research in this area has proceeded blind of these ideas. Rice’s (1996) seminal article has been cited approximately 150 times in the scientific literature but not once in a journal concerning human reproduction or fertility. Where evident, the prevailing functional framework in this literature starkly contrasts with sexually antagonistic coevolution: that reproduction is characterized by a cooperative division of labor in which the sexes have similar if not identical interests in the endeavor (e.g., Denison et al., 1999).

One piece of evidence is mildly suggestive of antagonistic coevolution. Female immunological responsivity appears to vary across the menstrual cycle. Cervical production of immunoglobulin A, the major immunoglobulin responsible for humoral immune reactions in the reproductive tract, is greatest 2 to 3 days prior to ovulation (Kutteh et al., 1996), days associated with peak fertility (Wilcox et al., 1995). Furthermore, antigen presentation by mucousal tissues in the reproductive tract is highest in the days just prior to ovulation, a time at which copulation can lead to conception (though it falls at ovulation itself; Prabhala and Wira, 1995). If female interests were driven solely by trade-offs between immune defense and fertilization, one would expect that immunocompetence would be reduced as fertility risk increased. The fact that certain forms of immunocompetence increase at high fertility risk suggests that other factors operate. As discussed above, ancestral females were more likely to have sex with extra-pair males near midcycle, mates who (1) probably were more likely to present novel STDs to females than their in-pair mates and (2) because of their lower likelihood of having multiple offspring with the female would be in greater conflict with her over level of immunosuppression. Possibly, then, women accord-

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

ingly evolved to increase their allocation of effort toward reproductive tract immune function during this time. An interesting and testable empirical question is whether men counter by increasing seminal levels of immunosuppressive factors when their mate is near mid-cycle. Such a pattern would constitute strong evidence for a coevolutionary tug-of-war between the sexes, quite possibly over female immune function.11

If male and female efforts to control immune function have antagonistically coevolved, we should expect rapid evolution and notable genetic variation of male seminal products and female immunological factors in the reproductive tract. We should furthermore expect that the struggle for control not infrequently leads to poor outcomes, either in the form of infertility or compromised female defense against STDs. Finally, the success of outcomes should partly be a function of the match between male ability to suppress female immune function and female ability to maintain it. These predictions may be explored in future research.

Conflict Over Parenting Effort

A large literature on the transition to parenthood has accumulated over the past two decades—the transition that individuals and couples experience during pregnancy, birth, and rearing of a first child (for a review, see, e.g., Gottman and Notarius, 2000). A robust finding across a large number of studies and multiple cultures is that, on average, men’s and women’s satisfaction with their marriages and their partners declines during the year following the birth of a first child (e.g., Terry et al., 1991; Crohan, 1996; El Giamal, 1997; Bottcher and Nickel, 1998; Gloger-Tippelt and Huerkamp, 1998; Morse et al., 2000; Wadsby and Sydsjo, 2001). As should be expected if explicit or implicit negotiation over responsibilities for child care and other household tasks entails conflicts, declines in marital satisfaction appear to substantially if not largely stem from perceptions that the partner does not meet expectations of responsible sharing in child care or that household tasks are allocated unfairly (Belsky and Hsieh, 1998; El Giamal, 1997; Grote and Clark, 2001).

If sexual conflicts of interest affected the evolution of negotiation strategies involved in these conflicts, we should perhaps expect that these conflicts revolve around the father’s allocation of time and effort to parenting

11  

The possibility that female immune responses against sperm are not merely a by-product of selection for defense against pathogens but rather are partly due to selection for their own benefits should also be considered. Lu and Zha (2000) found that seminal plasma from men with normal sperm inhibited antisperm antibodies more effectively than seminal plasma from men with abnormal sperm. Possibly, then, production of antisperm antibodies is a means whereby females increase the probability of conceiving with men with normal sperm.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

more so than the mother’s. As noted above, in most mammalian species (probably including humans), males pay a heavier cost of mating (searching for and attracting mates) than do females. Hence, even if both sexes may be motivated to engage in extra-pair mating, males in all likelihood pay a larger cost to seek it. As a result, the conflict over allocation of time and effort to parenting a new child is more likely to be around a father’s allocation of time to it (as opposed to effort to seek or attract new mates) than a mother’s (though it should be emphasized that mothers may provide or withhold care as tactics in the negotiation process). A number of findings are consistent with this expectation. Terry et al. (1991) found that an increase in females’ marital satisfaction across the transition to parenthood was predicted by a perception that her partner fairly participated in household tasks. Furthermore, a decline in women’s affection for their partners was evident only for those dissatisfied with their partner’s postpartum performance as a father and cooperative caretaker. By contrast, there was no evidence that men’s marital dissatisfaction was predicted by how well they perceived their partner’s performance as a mother. Similar findings were reported by Shapiro et al. (2000). In a study of couples from diverse socioeconomic backgrounds, Levy-Shiff (1994) found that fathers’ caregiving, play, and affiliative behaviors predicted stable or positive (as opposed to declining) marital satisfaction of both sexes. Maternal behaviors did not similarly predict satisfaction. (In fact, mothers’ caregiving actually predicted men’s marital satisfaction negatively, perhaps because it reflected greater caregiving by fathers themselves.) Rholes et al. (2001) reported that women preoccupied with concerns over their partners’ love and commitment to them who also entered parenthood concerned about the level of support they would receive from their husbands experienced particularly large declines in marital satisfaction. Again, no such effects were found for men. Finally, a study of Turkish couples with young first-born children revealed that a pattern of resolving conflicts (presumably often over child care and other household responsibilities) favoring the wife was associated with greater satisfaction of both spouses with their marriages; a pattern of conflict resolution in which the husband’s view prevailed predicted negative feelings toward the spouse (Hortacsu, 1999). These findings need not suggest that paternal involvement in child care and household responsibilities directly and unconditionally affects both parents’ satisfaction. They are consistent with the possibility that circumstances that favor paternal interest in participating in child care and household responsibilities lead to reduced conflict and increased marital satisfaction in these circumstances. (Factors that may influence paternal interest in participating in child care and household responsibilities are discussed below.)

Conflicts ultimately arising from diverging interests of the sexes per-

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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-

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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.

Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
×

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.

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Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
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Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
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Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
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Suggested Citation:"8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility." National Research Council. 2003. Offspring: Human Fertility Behavior in Biodemographic Perspective. Washington, DC: The National Academies Press. doi: 10.17226/10654.
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Despite recent advances in our understanding of the genetic basis of human behavior, little of this work has penetrated into formal demography. Very few demographers worry about how biological processes might affect voluntary behavior choices that have demographic consequences even though behavioral geneticists have documented genetics effects on variables such as parenting and divorce. Offspring: Human Fertility Behavior in Demographic Perspective brings together leading researchers from a wide variety of disciplines to review the state of research in this emerging field and to identify promising research directions for the future.

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