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Behavior Genetics, Vol. 33, No. 2, March 2003 (© 2003)
Mate Choice, Sexual Conflict, and Evolution of Senescence
Daniel Promislow1,2
Sex-related differences in longevity are common throughout the animal kingdom. Previous studies have suggested that at least part of these differences may be due to sex-specific costs of reproduction. Recently, workers have recognized that sexual conflicts of interest between males
and females may play a significant role in the evolution of sexually dimorphic traits. Here I
explore the possibility that sexual conflict may explain sex-specific differences in longevity and
may act as a driving force in the evolution of senescence. I present comparative evidence for
this hypothesis and discuss the potential relevance of sexual conflict theory to the search for
specific genes that influence longevity. One implication of a sexual conflict theory of aging is
that genes that influence senescence, and in particular those that affect sex differences in aging,
may evolve very rapidly and so be difficult to detect.
KEY WORDS: Sexual conflict; senescence; aging; sex-specific mortality; cost of reproduction.
2001). Whatever the cause for these sex differences,
they are apparent even among fetuses and newborns
(McMillen, 1979).
Differences in survival between males and females
turn out to be widespread in the animal kingdom,
though patterns vary among taxonomic groups. In most
mammal species, females live longer than males
(Promislow, 1992), whereas in birds, males typically
outlive females (Promislow, Montgomerie, and Martin,
1992). In fruit flies, patterns of sex-specific survival
vary from species to species (Promislow and Haselkorn,
2002) and depend on whether one is comparing
longevity in mated individuals or in virgin flies (e.g.,
Partridge and Andrews, 1985; Partridge, Green, and
Fowler, 1987; Sgrò and Partridge, 1999).
In the following paper, I discuss three aspects of
reproductive behavior that might influence sex-specific
differences in mortality. These factors include the
short-term physiological costs of reproduction and
the longer-term evolutionary consequences of female
mate choice and sexual conflict. I will also discuss
evidence for sex-specific genes that influence fitness and
how reproductive behavior might affect the evolution
of these genes.
An earlier study (see Svensson and Sheldon, 1998)
noted that sexual conflict could lead to increased
INTRODUCTION
Women have longer life expectancies than men in 190
of 205 populations around the world, with an average
advantage of 4.4 years (2002 data, Population Reference Bureau, http://www.prb.org). In developed countries, this difference may exceed a decade. Of course,
this dramatic difference has not gone unnoticed, as
shown by the very popularity of the title “Why Do
Women Live Longer Than Men?” in the scientific literature (e.g., Epstein, 1983; Grut, 1998; Hazzard, 1989;
Holden, 1987; Promislow, 1991b; Schneider, Cebrat,
and Stauffer, 1998; Seely, 1990; Waldron, 1976, 1978).
In humans, one common answer to the question of
why females live longer than males is that they differ
in their hormone profiles. For example, high levels of
testosterone are associated with increased aggression,
which could lead to higher mortality among males
(Book, Starzyk, and Quinsey, 2001). At the same time,
high levels of estrogen in women may actually reduce
mortality rates (Reis et al., 2000; Rodriguez et al.,
1
2
Department of Genetics, University of Georgia, Athens, GA 30602–
7223, USA.
To whom correspondence should be addressed at Tel: (706) 5428000. Fax: (706) 542–3910. e-mail:[email protected]
191
0001-8244/03/0300-0191/0 © 2003 Plenum Publishing Corporation
192
mortality rates. Here I develop this argument more
fully, arguing that sexual conflict between males and
females may account not only for sex differences in
mortality but also for the evolution of senescence itself.
Given recent advances in our theoretical understanding
of sexual conflict, its macroevolutionary patterns and
molecular genetic consequences, the ideas presented
here should soon be experimentally testable.
MORTALITY AND COSTS OF
REPRODUCTION
The most direct effects of reproduction on mortality rates are seen in the physiological costs of mating, gamete production, and parental care. In many
species, behaviors associated with reproduction have
been shown to decrease life expectancy (Reznick,
1985). Studies in Drosophila, in particular, have demonstrated that courtship behavior, copulation, and gamete
production can all lead to higher mortality rates in both
males and females (Partridge, 1980, 1987; Partridge
and Andrews, 1985; Partridge and Farquhar, 1981;
Partridge and Harvey, 1985; Sgrò and Partridge, 1999).
All of these behaviors are energetically costly, so it is
not surprising that they have deleterious effects on
longevity.
There is some debate as to whether costs of reproduction affect humans as well. In wealthy societies,
high resource levels may offset any costs of reproduction. However, throughout human history, there has
clearly been an increased risk of mortality during childbirth (Loudon, 1993), and comparisons both within and
among populations point to a negative correlation between number of children and life span (Lycett, Dunbar,
and Voland, 2000; Thomas et al., 2000; Westendorp
and Kirkwood, 1998). Although it is likely that increased reproductive output increases mortality rates,
it is not clear how these costs could account for the
greater life expectancy seen in women. Perhaps in the
absence of reproductive costs, the sex difference in
longevity would be even greater.
Nevertheless, many of the most successful attempts
to extend longevity in model organisms point to the
importance of reproduction in the aging process. For
example, studies in both flies and rodents have demonstrated that caloric restriction can dramatically extend
life span (Masoro, 2000; Nusbaum and Rose, 1999).
Animals that are fed a calorically restricted diet have not
only higher survival but also increased stress resistance
and increased activity levels (e.g., McCarter et al.,
1997). However, calorically restricted individuals also
Promislow
show a dramatic reduction in reproductive capacity. This
loss of reproductive ability could account for the increase in longevity. In fact, some have argued that this
may be an adaptive response to living through lean
times (Holliday, 1989; Masoro and Austad, 1996).
More recently, biogerontologists have shown that
diapause, in which an animal enters a state of reproductive stasis, can also stop or slow the aging process
(Herman and Tatar, 2001; Tatar et al., 2001; Tatar and
Yin, 2001). For example, many of the genes that have
been shown to extend longevity are involved in dauer
formation in nematodes (Guarente and Kenyon, 2000)
(the nematode equivalent of diapause) or in adult diapause in flies (Clancy et al., 2001; Tatar et al., 2001).
Given that reproduction may mediate the ties between
aging and both caloric restriction and diapause, it may
turn out that scientists working on the genetics of aging
may actually be working on the genetics of reproduction.
This claim is further supported by the finding that
some loci are associated with longevity in one sex but
not the other (Nuzhdin et al., 1997). These sex differences may well be due to sex-specific differences in
reproductive physiology.
Experimental evidence suggests that reproductive
behaviors can both increase and decrease longevity.
Some studies suggest that mate choice, whereby females
choose to mate with fitter-than-average males, can
increase life span, though the effect is relatively weak
(Partridge, 1980; Promislow, Smith, and Pearse, 1998).
On the other hand, genotypes that increase fitness in
one sex may actually reduce fitness in the opposite sex
(Rice and Chippindale, 2001). These sex-specific
genetic effects may arise due to reproductive conflicts
of interest between males and females. In the following sections, I explore how costs and benefits of
reproductive behaviors might influence the evolution
of sex differences in life span.
MATE CHOICE, SEXUAL CONFLICT, AND
SEX DIFFERENCES IN AGING
Mate Choice
Over a century ago, Charles Darwin and Alfred
Russell Wallace recognized that female mate choice of
males and male-male competition for access to females
played an important role in the evolution of sexually
dimorphic traits (Darwin, 1871; Wallace, 1889). These
elaborate traits include a range of morphological and
behavioral factors, such as large antlers in deer, elaborate and colorful plumage in birds, and the complex,
Mate Choice, Sexual Conflict and Senescence
ritualized courtship behaviors found throughout the
animal kingdom. These traits may allow males to attract
females or to compete successfully against other males
and so increase reproductive success, but they also can
exact costs. A brightly colored bird not only is more
likely to attract females but also must pay the physiological costs of producing and maintaining the bright
plumage and will be more conspicuous to predators
(Andersson, 1994).
Biologists have explored a range of possible explanations to try to understand the forces that could
maintain these costly traits. One argument is that males
vary in quality (e.g., viability, fertility, or competitive
ability), and elaborate traits signal a male’s quality to
the female (Andersson, 1994).
From a gerontological perspective, this model has
interesting implications. If a cohort of young males
varies in some aspect of quality, and if this quality
influences the probability of survival, then as males get
older, their underlying viability (notwithstanding the
effects of aging) should improve. As a cohort ages, the
lowest-quality individuals will die off first. On average, older males will have better-quality genes to pass
on to their offspring. Thus, if a female can choose
among males based on age, by choosing to mate with
an older male, she is more likely to pass on high-quality
viability genes to her offspring.
Theoreticians have examined the conditions under
which preference for old mates can evolve (Beck and
Powell, 2000; Hansen and Price, 1995; Kokko and
Lindström, 1996). Only recently, however, have biologists asked whether preference for older males can
actually influence the evolution of aging. In a recent
theoretical study, Beck et al. (2002) carried out simulations in which a cohort of females was allowed to
evolve varying degrees of preference for males of different ages. Typically, after many hundreds of generations, females would evolve a bias against young males
and in favor of older males (Fig. 1). But there was an
interesting consequence of this preference. The authors
compared mortality rates in cohorts where females were
allowed to exercise their age-specific mate preference
with cohorts of females that were forced to mate at random. After many generations, the mortality rates in
the “choosy” cohort were significantly lower than in
the random mating cohort (Fig. 2). By choosing to mate
preferentially with older males, females can improve
the chances that they produce high-quality offspring.
At the same time, female preference for older males
can increase the frequency of genes for high viability
and the strength of selection acting at late ages, thereby
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Fig. 1. Female preference based on male age. In a genetic algorithm
simulation, Beck et al. (2002) found that females evolved a preference for older males, except at very high mortality rates, where
females preferred to mate with males of intermediate age. Preference
refers to the probability that a female will mate with a randomly
encountered male of a particular age. The three curves represent
simulations for populations with low (thick line), medium (thin line),
or high (dashed line) rates of increase in age-specific mortality (figure
based on data reported in Beck et al. 2002).
Fig. 2. Effect of female preference on average mortality in populations with and without age-specific mate preference. The y-axis
shows the natural log of the initial mortality rate in the population,
where mortality rates increase exponentially with age. Smaller (more
negative) values imply lower mortality rates. Comparisons between
populations with and without female preference are shown for three
levels of senescence, with senescence determined by the rate of
increase in mortality rates with age. In populations where females
are allowed to choose mates, mortality rates evolve to a lower equilibrium value (figure based on data reported in Beck et al. 2002).
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having the long-term, unintended consequence of
increasing life span of the entire cohort.
The theoretical finding that female choice can
extend longevity over evolutionary time is supported
by experimental and comparative data. Promislow,
Smith, and Pearse (1998) used artificial selection to
create divergent lines with high and low levels of opportunity for mate choice and male-male competition.
They found that populations with greater levels of sexual selection evolved a longer life span. In a comparative study of mortality rates and plumage coloration,
Promislow, Montgomerie, and Martin (1992) found that
bright coloration was more likely to be found in species
with high female survival rates. At the time, the authors drew the causal arrow from mortality to coloration, arguing that high mortality rates would act as
a constraint on the evolution of costly secondary sexual characteristics. However, Beck et al. (2002) suggest another possibility. If bright plumage is an indicator of quality, then in brightly colored species,
females will have the opportunity to choose males with
genes that increase viability, and over evolutionary
time, survival rates will increase.
Sexual Conflict
Mating behavior may reduce mortality rates over
evolutionary time, but it is not without costs. These
costs may arise due to inherent conflicts of interest
between the sexes. In mating contests between males
and females, what is optimal for one sex may be suboptimal for the other sex. Consider sperm competition
as an example. In many species, females will mate with
two or more males in relatively quick succession.
Sperm from multiple males are thus competing for
access to the female’s eggs. Selection will favor males
that are most able to displace sperm from previous
males, and to avoid being displaced by subsequent
males. At the same time, selection may favor females
that are able to control which sperm fertilizes their
eggs. Due to these conflicts of interest between the
sexes, traits that increase fitness in males could, theoretically, decrease fitness in females.
A series of studies has now shown that natural
selection can favor males that actually harm their mates,
reducing their survival rates quite dramatically (Chapman et al., 1995; Rice, 1996). In many circumstances,
mating behaviors, and even specific genes, that are
optimal for one sex may be deleterious for the other
sex, leading to sexual conflict (Partridge and Hurst,
1998; Rice, 2000; Rice and Chippindale, 2001).
Promislow
These conflicts between the sexes could potentially lead to increased mortality rates in females
(Svensson and Sheldon, 1998). Fruit flies provide a
powerful model to study the genetics and evolution of
sexual conflict and aging. Female fruit flies typically
mate with two or more males. In the race to fertilize
eggs, males have evolved proteins that appear to incapacitate sperm from previous males (Price, Dyer, and
Coyne, 1999) or to prevent their sperm from being displaced by subsequent males (Clark et al., 1995). But a
male can also improve his fitness by manipulating
female behavior. In flies, the last male to mate with a
female fertilizes most of the eggs the female is carrying
at that time. To increase the probability of fertilizing a
female’s eggs, males produce specialized substances
(accessory gland proteins, or Acps—Wolfner et al.,
1997) that reduce receptivity of the female to subsequent courting males and force the female to lay more
eggs than might be optimal from the female’s perspective (Wolfner et al., 1997). In this way, a male can
increase the relative number of eggs fertilized by his
sperm.
However, Acps not only alter a female’s mating
behavior but also increase her risk of dying. In a 1995
study of Drosophila, Tracy Chapman and colleagues
(1995) mated females with normal males and with
males that do not produce Acps. Only females exposed
to Acps showed increased mortality. At least one candidate gene, Acp62F, has been identified as a possible
cause of increased female mortality. The Acp62F protein is similar to proteinase inhibitors found in nematodes (Lung et al., 2002), and part of its structure is
similar to a neurotoxin produced by the Brazilian armed
spider, Phoneutria nigriventer (Wolfner et al., 1997).
It is unlikely that natural selection has led to the
evolution of proteins whose sole purpose is to increase
female mortality rate. Rather, the benefits that Acps
provide in terms of increased male reproductive success outweigh the costs (from the male’s perspective)
of increased female mortality. Since females do not
appear to benefit from this situation, should they not
evolve some response to disable the effect of male
Acps? In fact, a study by Rice suggests that such
coevolutionary responses do occur. Rice (1996) developed an experimental procedure in which males were
selected for high mating success in competition with
other males, but females were prevented from responding genetically to changes in males. Within a few
tens of generations, he found that males had evolved
much higher reproductive success than unselected control lines. More important, when mated with females,
Mate Choice, Sexual Conflict and Senescence
experimental males induced much higher female mortality rates than did the control males.
Thus, it appears that males are continually evolving ways to maximize their sperm competitive ability,
including processes that manipulate female behavior or
physiology, and females are evolving counteradaptations to prevent being manipulated by the male. These
conditions set the stage for a continual arms race
between males and females. At times, we expect males
to gain the upper hand, while at other times females
will have the advantage (Fig. 3).
This arms race points to one possible reason why
in some species males might have higher mortality
than females, whereas in other species the reverse
would be true, depending on which sex has the current advantage. This pattern of males winning the
arms race in some species and females in others is
illustrated by a recent study across species of water
strider (Arnqvist and Rowe, 2002). Male water striders have evolved grasping hooks to hold on to females
during copulation, and females have evolved spines
to ward off unwanted suitors. In species where females have the upper hand in competition with males,
females have large spines, and copulations are relatively short. When males hold the advantage, hooks
are proportionately larger than spines, and copulation
duration increases.
The size of hooks and spines is easy to measure.
The biochemical shape of Acps that influence mating
behavior in flies is not so easily measured but may
exhibit the same pattern of adaptation and counteradaptation as seen in water striders. At present, we can-
Fig. 3. Sexual conflict can lead to states where females have higher
fitness than males or vice versa. This may account, at least in part, for
the sex bias in adult mortality (Chippindale, Gibson, and Rice, 2001).
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not take a biochemical snapshot of the arms race among
different species of Drosophila, though experiments
such as that of Rice (1996), described earlier, provide
evidence that genetic variation exists for such
macroevolutionary patterns to arise. It remains to be
determined, however, if we can extrapolate from fruit
flies to humans. Like flies, human males have an impressive assortment of glands that contribute to seminal fluid. Birkhead (2000) makes a fairly convincing
argument that at least some of these glands have
evolved under the force of sexual conflict. We do not
yet know whether human males produce seminal products that manipulate females, though other sorts of
manipulation is certainly likely (Gowaty, 1997). Interestingly, a comparative study in primates provides some
evidence that these accessory glands play a role in
sperm competition (Dixson, 1998).
By definition, sexual conflict implies that one sex
suffers when the other gains. Until now, we have considered the possibility that sexual conflict may influence sex biases in mortality. But it might also lead to
the evolution of senescence itself. Just as sexual conflict has driven the evolution of ever-increasing trait
size in male and female water striders (Arnqvist and
Rowe, 2002), the same process could lead to increasing mortality rates in both sexes of a species where sexual conflict is pervasive. In the context of sexual conflict, males and females not only will evolve traits that
harm one another but also will pay the cost of bearing
these complex traits. As the sexual conflict arms race
progresses, the costs of these traits should continually
increase, so that species with relatively high levels of
sexual conflict would have relatively high mortality
rates (see Johnstone and Keller, 2000).
Most evolutionary models of aging suggest that
high intrinsic mortality rates will select for high rates
of senescence (Charlesworth, 1994; Ricklefs, 1998; but
see Abrams, 1993). (By “rate of senescence,” we mean
the rate at which mortality rates increase with age
[Finch, Pike, and Witten, 1990; Promislow, 1991a]).
Thus, if sexual conflict increases mortality rates, this
could lead indirectly to the evolution of senescence. At
the same time, in a process that is akin to Medawar’s
mutation accumulation model, females may counteract
the costs of male traits arising due to sexual conflict by
delaying their effects until later in life. This could lead
to increased mortality rates at late age in females,
though it is not clear how this might translate into
higher rates of aging in males.
The interrelationships of female preference, male
ornaments, sexual conflict, underlying demography,
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and so forth are likely to be rather complex (Fig. 4). In
the future, formal mathematical models should explore
the demographic and behavioral conditions under
which sexual conflict could lead to the evolution of
senescence. For now, the following section provides
examples from various species suggesting that sexual
conflict could explain interspecific variation in life history strategies in general, and life span in particular
(see also Svensson and Sheldon, 1998).
Sexual Conflict and the Evolution of Aging—
Comparative Evidence
Arnqvist and Rowe (2002) demonstrated how
comparative approaches could be used to examine the
consequences of varying degrees of sexual conflict
among species of water strider. To test the hypotheses
presented here, ideally we would compare the extent
of sexual conflict among species with measures of mean
life span, sex-specific mortality rates, and rates of
senescence. While there are plenty of published data
on survival rates, measuring sexual conflict turns out
Promislow
to be rather difficult (water striders notwithstanding).
Bearing this challenge in mind, I discuss several biological factors that may lead to reduced levels of sexual conflict and that also appear to be associated with
reduced mortality rates.
Eusociality
In eusocial species of ants, bees, and termites,
queens can be extremely long-lived, surviving upwards
of 20 years (Keller and Genoud, 1997). Keller and
Genoud (1997) suggest that long life span in eusocial
species is due to the highly sheltered environment in
which queens live. Carey (2001) places the cause
directly in the behavioral realm. I extend his explanation to include the possibility of sexual conflict.
While conflicts of interest between queens and
workers or between workers and males are common
(Hamilton, 1964; Sundstrom and Boomsma, 2001),
species with single queens tend to have extremely low
levels of sexual conflict between the queen and her
Fig. 4. Possible pathways for mate choice and sexual conflict to influence the evolution of senescence. For example, female mate choice could
increase mortality rates if mate choice led to the evolution of costly secondary sexual characteristics. On the other hand, females choice could
decrease mortality if females selected males with genes for high viability. Sexual conflict could lead to high mortality rates (see text), but in
species where females have relatively high levels of control over the conflict, the consequences of sexual conflict might be reduced.
Mate Choice, Sexual Conflict and Senescence
mates. Queens typically mate with one or multiple
males on a single mating day, after which the queen
founds a colony. To fertilize offspring, the queen uses
sperm that have been stored for years or even decades
after this first mating bout.
In this situation, there should be strong selection
on males to prevent them from evolving mechanisms
that kill off or displace sperm from other males and that
harm the female, and strong selection on females to
evolve countermeasures to harmful male traits. A
queen’s fitness depends on her ability to produce a large
colony and to have sperm in sufficient numbers to last
many years. Thus, a male may actually benefit by deliberately not increasing female mortality or, in the case
of polyandrous queens, by not displacing sperm from
previous males. The more sperm a female carries and
the longer she lives, the greater the chance that a male’s
sperm will fertilize offspring that will, themselves,
eventually become queens.
Monogamy
In a lifelong monogamous species, males and
females will have concordant strategies to maximize
fitness, and sexual conflict should be absent or slight
(Rice, 2000). Even when there is some conflict, such
as in socially monogamous species that seek extrapair
copulations outside the pair bond (Gowaty, 1996), levels
of conflict are still likely to be lower than in polygamous species, so we would expect monogamous species
to be longer-lived or to have lower rates of aging. Some
evidence from mammals supports this argument. While
most mammals are polygynous and show significant
evidence of aging, in monogamous species of canids,
rates of senescence are conspicuously low (Promislow,
1991a).
Postreproductive Survival
Over the past decade, biodemographic studies have
shown that at very late ages, the age-related rate of
increase in mortality slows and may show a reversal in
fruit flies, nematodes, and even humans (Carey et al.,
1992; Curtsinger et al., 1992; Vaupel et al., 1998). As
reproduction slows down or ceases altogether at late
age, so, too, does the amount of sexual conflict. In
Drosophila, for example, if older females no longer
mate (or are housed with males that no longer mate),
they may no longer pay the cost of exposure to Acps.
Thus, sexual conflict could account for mortality
deceleration seen in many species.
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Cooperative Breeding
In many species of birds, mature offspring forgo
the opportunity to breed and instead remain at the natal
nest for one or more seasons, helping their parents to
rear younger siblings or half siblings. Work on the
extraordinarily promiscuous Australian fairy wren suggests one way in which helpers at the nest can reduce
the costs of sexual conflict. If females mate outside the
pair bond, males may be less likely to help rear offspring due to uncertain paternity (Møller and Birkhead,
1993). In the fairy wren, it appears that this cost is offset by the presence of helpers at the nest (Mulder et al.,
1994), giving females an advantage in conflicts with
mates. Within the general framework of cooperative
breeding, there is a wide range of mating systems
(Cockburn, in press). Whether the costs to females of
sexual conflict are generally reduced in cooperative
breeders remains to be seen. But in line with the theory developed here, comparative evidence shows that
cooperative species do tend to have lower mortality
rates (Arnold and Owens, 1998; Møller and Birkhead,
1993).
Sexual Conflict and the Evolution of Aging—
Experimental Tests
At least one study in fruit flies has shown experimentally that increasing the opportunity for sexual
selection leads to an increase in adult survival (Promislow, Smith, and Pearse, 1998). However, this study was
not a test of a sexual conflict theory of aging per se,
since flies were not allowed to mate multiply. In the
absence of multiple mating, sexual conflict is greatly
reduced, at least in flies. Fortunately, there are several
ways in which we can reduce opportunity for sexual
conflict. Using a variety of techniques, several studies
have shown that increased conflict shortens life span
(Chapman et al., 1995; Holland and Rice, 1999; Rice,
1996). These studies suggest a way that might explore
directly the relationship between sexual conflict and
rates of aging.
Earlier, I noted that Acps play a central role in the
Drosophila male’s ability to manipulate female
reproductive behavior and physiology. Wolfner et al.
(1997) have created strains in which males do not produce any Acps. To test the idea that sexual conflict
leads to the evolution of aging, one could simply maintain large, outbred populations of flies with and without the presence of Acps. If sexual conflict increases
mortality rates, then the populations without Acps
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should gradually evolve longer life span relative to
those that do produce Acps.
Challenges for a Sexual Conflict Theory of Aging
The link between sexual conflict and senescence
is still conjectural at this point. The examples discussed
here provide support for the novel hypothesis that increases in sexual conflict play an important role in the
evolution of increased rates of aging and/or decreased
longevity (see also Svensson and Sheldon, 1998). However, we have yet to obtain direct experimental evidence, and there are alternative explanations for each
of the comparative examples presented here. For example, eusocial ants tend to live in environments that
are well protected from predators and climatic fluctuations. In cooperatively breeding species, individuals may live longer simply because they can help
each other with the important tasks of daily living.
The advantage of the sexual conflict hypothesis is that
it pertains to multiple ecological situations and is
experimentally testable.
In fact, there are three distinct cross-specific patterns that need to be explained. Species differ in mean
life span (e.g., Gaillard et al., 1989), in the degree to
which mortality rates increase with age (Promislow,
1991a; Ricklefs, 1998), and in the degree of sex bias
in mortality (Clutton-Brock, Albon, and Guinness,
1985; Promislow, 1992; Promislow, Montgomerie, and
Martin, 1992). Future theory should consider the possibility that each of these three patterns could be influenced by interspecific variation in the strength of
sexual conflict.
Promislow
for longevity and may also suggest something about the
nature of genes that influence aging.
When genes increase or decrease fitness equally
in both sexes, natural selection leads to the fixation or
loss of these genes. Genes involved in sexual conflict,
however, increase fitness in one sex at the expense of
fitness in the opposite sex. This antagonistic effect is
expected to generate negative genetic correlations for
adult fitness in males and females and can maintain
polymorphisms for fitness-related genes in natural
populations.
Rice and Chippindale (2001) use the example of
the human hip to illustrate this argument. Natural selection should favor relatively large hip size in women
to facilitate easy passage of the fetus through the birth
canal. Increased hip width may decrease locomotor performance, but females gain the benefit of decreased
complications at birth. Males, on the other hand, gain
no such direct benefit. Thus, selection should favor alleles that increase hip width in females but decrease
hip width in males, setting the stage for conflict. In an
experimental test of this idea, Chippindale, Gibson, and
Rice (2001) used “clone generator” females to create
large numbers of males and females that shared an identical set of major chromosomes. This allowed the researchers to determine the effects on fitness of identical
genotypes in a male or female background. Consistent
with sexual conflict theory, Chippindale, Gibson, and
Rice (2001) found that among forty different Drosophila
genomes, genotypes that increased relative fitness in
males tended to decrease fitness in females. Although
not the focus of their study, this result supports the
contention that sexual conflict could maintain genetic
variation for longevity in natural populations.
Sexual Conflict and Genetic Variation
The strength of selection tends to be strongest on
fitness traits, such as fecundity or survival, and so over
time, selection should erode genetic variation for these
traits as deleterious alleles are lost and beneficial ones
go to fixation (Fisher, 1930). But there remains plenty
of genetic variation for life span (Rose, 1991). What
maintains this variation? Classic evolutionary theories
of senescence suggest two possibilities. Genetic variation for longevity is maintained either by the lack of
selection acting on genes whose effects are limited to
late ages (mutation-selection balance; Medawar, 1952)
or because some genes that decrease survival late in
life have beneficial effects early in life (antagonistic
pleiotropy; Williams, 1957). Sexual conflict provides a
third hypothesis for the maintenance of genetic variation
Sexual Conflict: Why Should Molecular
Biogerontologists Care?
We have established that costs of reproduction can
increase mortality rates. We have seen how one sex can
manipulate the other, using either morphological or biochemical means, and so increase the mortality rate of
the manipulated sex. And recent studies have demonstrated that at least some genes that increase fitness in
one sex may decrease it in the other. These results suggest three ways in which gerontological research could
benefit from thinking about the causes and consequences of sexual conflict.
First, studies on the genetics of sexual conflict
(Chippindale, Gibson, and Rice, 2001; Rice, 1992,
1998) point out that many important genes may have
Mate Choice, Sexual Conflict and Senescence
sex-specific effects and may even increase fitness in
one sex while decreasing it in the other. The search for
aging genes is often confined to the study of a single
sex. In several recent, widely cited examples of genes
that extend longevity (Lin et al., 1998; Parkes et al.,
1998; Rogina et al., 2000), data on survival were provided for males only. More comprehensive experiments
are necessary.
Second, we have identified numerous genes that
appear to be involved in sexual conflict, including
accessory gland proteins in Drosophila (Wolfner et al.,
1997), and recent studies suggest that both X- and Ylinked loci may be especially important for sex-specific
fitness traits (Chippindale and Rice, 2001; Gibson,
Chippindale, and Rice, 2002). These may be useful
candidate loci in the search for longevity genes.
Finally, classical population genetics theory suggests that genes that extend longevity should go to
fixation. Thus, we should expect to find little genetic
variation for life span in natural populations. Data from
humans and many other species contradict this expectation, so we are left with the problem of what maintains this variation. One possibility is that genes that
extend longevity have antagonistic pleiotropic effects,
decreasing fertility or fecundity. However, some studies have found genes that increase life span but do not
decrease reproductive capacity (Lin, Seroude, and Benzer, 1998). It may turn out that a significant amount of
segregating genetic variation for life span is maintained
by balancing selection created by sexual conflict. Genes
involved in sexual conflict may turn out to be excellent candidates for studies on the genetics of aging.
However, this also points to a very important caveat.
Genes involved in sexual conflict tend to evolve very
quickly (Swanson et al., 2001). To the extent that these
rapidly evolving genes influence longevity, the search
for aging genes may turn out to be the search for a
moving target.
ACKNOWLEDGMENTS
Thanks to A. Keyser and C. Spencer, who provided
helpful comments on an earlier draft of this manuscript.
Useful comments were also provided by J. Harris and
two anonymous reviewers. This work was supported by
National Institute on Aging grant AG14027.
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