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8. Sexually Antagonistic Coevolution: Theory, Evidence, and Implications for Patterns of Human Mating and Fertility
Pages 224-259

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From page 224...
... 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.
From page 225...
... 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. IT'S · 1 1 1 · TO - T 1 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.
From page 226...
... 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.
From page 227...
... 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.
From page 228...
... 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.
From page 229...
... 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~.
From page 230...
... 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.
From page 231...
... . In the case of sexually antagonistic adaptations, however, rapid evolution may lead to variation being maintained.
From page 232...
... 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.
From page 233...
... , 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)
From page 234...
... and genetic benefits (benefits that indirectly increase female reproductive success by increasing the viability or 4As discussed later, multiple matings by both males and females can increase sexual conflicts of interest regarding parental investment.
From page 235...
... . J antagonistic interaction, as discussed In this papery; t2' 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)
From page 236...
... 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.
From page 237...
... 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.
From page 238...
... . 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.
From page 239...
... 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.
From page 240...
... 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.
From page 241...
... 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.
From page 242...
... . ~ ton envoy Ping maternal Imprinting.> We should expect that, like other antagonistic coevolutionary processes, the coevolution of imprinting should yield the evolutionary outcomes discussed earlier.
From page 243...
... 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.
From page 244...
... 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 lowleve!
From page 245...
... , 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.
From page 246...
... 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-ofwar. Evidence for such a tug-of-war could be that females counteract male immunosuppressive activity by, for instance, disabling those functions.
From page 247...
... Such a pattern would constitute strong evidence for a coevolutionary tug-of-war between the sexes, quite possibly over female immune function.ll 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.
From page 248...
... 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.)
From page 249...
... (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.
From page 250...
... These possibilities may be explored in future research. lust 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.
From page 251...
... 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)
From page 252...
... do sexual conflicts of interest fail to exist. Multiple matings by members of both sexes (whether serially or simultaneously)
From page 253...
... Proceedings of tI7e Royal Society of London B265:2393-2397.
From page 254...
... 2000 Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403:886-889.
From page 255...
... Experimental removal of sexual selection reverses intrasexual antagonistic coevolution and removes a reproductive load. Proceedings of the National Academy of Sciences USA 96:5083-5088.
From page 256...
... Hartley 2002 Intrafamilial conflict and parental investment: A synthesis. Philosophical Transactions of the Royal Society of London B357:295-307.
From page 257...
... Yip, and S.C. Mok 1998 Gene expression, immunolocalization, and secretion of human defensin-5 in human female reproductive tract.
From page 258...
... Woliner, and C.F. Aquadro 2001b Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.
From page 259...
... Prabhala, and C.R. Wira 1998 The mucosal immune system in the human female reproductive tract: Potential insights into the heterosexual transmission of HIV.


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