TREE-1830; No. of Pages 9
Review
Female extra-pair mating: adaptation
or genetic constraint?
Wolfgang Forstmeier1, Shinichi Nakagawa2, Simon C. Griffith3, and
Bart Kempenaers1
1
Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, 82319 Seewiesen, Germany
2
Department of Zoology, University of Otago, Dunedin 9054, New Zealand
3
Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia
Why do females of so many socially monogamous spe- should be evaluated, including models in which genetic
cies regularly engage in matings outside the pair bond? constraints prevent the evolution of optimal behaviour.
This question has puzzled behavioural ecologists for Adaptive hypotheses for female extra-pair mating have
more than two decades. Until recently, an adaptionist’s focussed on a range of possible benefits, yet there are
point of view prevailed: if females actively seek extra-
pair copulations, as has been observed in several spe- Glossary
cies, they must somehow benefit from this behaviour. Adaptive (adaptationist) hypothesis: explanations that a particular trait has
However, do they? In this review, we argue that adaptive evolved to increase an individual’s fitness (see ‘individual fitness’ below).
scenarios have received disproportionate research at- Antagonistic pleiotropy: when alternative genetic variants (alleles) affect
multiple phenotypic traits under opposing selection pressures (e.g., an allele
tention, whereas nonadaptive phenomena, such as has beneficial effects on trait 1 but detrimental effects on trait 2); such traits can
pathological polyspermy, de novo mutations, and ge- be found within one sex (intrasexual antagonistic pleiotropy), or across the
sexes (intersexual antagonistic pleiotropy); in the latter, it can be the same
netic constraints, have been neglected by empiricists
phenotypic trait expressed in each sex that is under opposing selection.
and theoreticians alike. We suggest that these topics Compatible genes: alleles that increase the fitness of an organism only when
deserve to be taken seriously and that future work would combined with a particular set of other alleles and, therefore, the fitness
benefits normally are not heritable; these alleles contribute to nonadditive
benefit from combining classical behavioural ecology genetic variance (e.g., epistasis), which is part of the phenotypic variance.
with reproductive physiology and evolutionary genetics. Genetic constraint: limitations to the adaptation of an organism due to its
genetic architecture.
Costs and benefits of female extra-pair mating Genetic correlation: correlation between two traits that arises from shared
genetic effects (because the traits are affected by the same alleles); such
Mating outside the social pair bond seems obviously adap- genetic correlation can be found within one sex (within-sex genetic correlation)
tive for males, but the benefit to females is less clear or across the two sexes (cross-sex genetic correlation; here, the genetically
correlated traits can be the same trait expressed in males and in females).
because it does not increase the number of offspring that
Good genes: alleles that directly increase the fitness of an organism, so that the
they produce. Given that active female extra-pair mating is fitness benefits are heritable; these alleles contribute to additive genetic
often found, behavioural ecologists have sought explana- variance, which is part of the phenotypic variance.
Individual fitness: the contribution of an individual to the gene pool of future
tions for this behaviour. Numerous adaptive explanations generations. Fitness benefits are often divided into direct (nongenetic) benefits
have been proposed [1,2], yet general support for these (e.g., obtaining food) and indirect (genetic) benefits (e.g., obtaining ‘good
hypotheses remains limited [3–5]. Most of the research has genes’). Note that, in the context of extra-pair mating, copulations do not have
to lead to extra-pair fertilisations for the female to obtain direct benefits [71].
been conducted in a framework of adaptionist thinking: Intralocus sexual conflict: when opposing selection pressures act on allelic
the fact that females show active extra-pair mating must variation at one gene locus, because one allele enhances the fitness of males
mean that they benefit from this behaviour. Nonadaptive whereas the other allele enhances the fitness of females.
Linkage disequilibrium due to assortative mating: nonrandom mating with
explanations [6] were rapidly discarded [7,8] and then regard to phenotypes (e.g., promiscuous females mate with promiscuous
apparently forgotten ([6] was not cited in the extra-pair males) leads to an association between alleles that influence those phenotypes
paternity literature between 1995 and 2011). However, (e.g., alleles for male promiscuity and alleles for female promiscuity will often
be found in the same individuals).
several of the most powerful empirical tests of adaptive Nonadaptive (maladaptive) hypothesis: explanations for the evolution or
explanations have yielded puzzling results [9–11], even maintenance of a particular trait or behaviour despite the fact that it decreases
suggesting that female extra-pair mating behaviour is the fitness of an individual (see ‘individual fitness’ above).
Oligospermy: male fertility condition that leads to scarcity of sperm cells,
detrimental to females (behaviour we refer to as maladap- which could result in a reduced ability or inability to fertilise eggs.
tive; see Glossary). Moreover, a first empirical test of a Polyspermy: more than one sperm cell penetrates the egg membrane, usually
due to an excessive supply of sperm. Fertilisation by more than one sperm leads
nonadaptive explanation [6] provided support for the idea
to a nonviable zygote because of an abnormal copy number of chromosomes
that female promiscuity could evolve even when it has (pathological polyspermy). In birds, typically many sperm penetrate the egg
negative consequences to females [12]. These two develop- membrane (referred to as physiological polyspermy) but typically the nucleus of
only one sperm fuses with the nucleus of the egg (hence, the analogue of
ments suggest that a broader spectrum of hypotheses pathological polyspermy in birds is polyspermic fusion of nuclei).
Polygenic trait: a character that is controlled by numerous loci (genes); in
Corresponding author: Forstmeier, W. (forstmeier@orn.mpg.de). contrast to a monogenic trait, which is controlled by one locus.
Promiscuity: used as short for an increased propensity to copulate with
0169-5347/
multiple individuals (also outside the pair bond); here not used to imply
ß 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2014.05.005
indiscriminate mating.
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Table 1. Possible benefits and costs associated with female extra-pair mating
Proposed benefits Refs Possible costs Refs
Good or compatible genes (genetic benefits) [1–4,72] De novo deleterious mutations [19,20]
Avoiding inbreeding (with related partner) [22,23]
Inclusive fitness gain by extra-pair mating with kin [73] Inbreeding depression [73]
Fewer infertile eggs (fertility insurance) [30] Increased embryo mortality (polyspermy) [37]
Avoid infanticide by other males [46] Punishment or aggression by social mate [74]
Reduced harassment (convenience polyandry) [5] Increased harassment (Box 3)
Increased care (by extra-pair males) [71] Loss of care (by social mate) [4]
Access to resources held by neighbours [75]
Securing a future partner [76] Risk of losing the current partner
Bet-hedging benefits via offspring diversity [77] Increased sibling competition [78]
Beneficial sexually transmitted microbes [79] Sexually transmitted diseases [13]
also many possible costs associated with this behaviour The third and most direct approach to test genetic
(Table 1). Some of these costs, such as the greater likeli- benefit models is to compare fitness-related traits of ex-
hood of contracting a sexually transmitted disease, have tra-pair young relative to those of within-pair young. Al-
been posited for several decades [13] and, yet, have been though many studies have suggested that extra-pair
largely ignored empirically. Most of these costs and ben- offspring do better in one way or another (e.g., survive
efits have been discussed extensively elsewhere (see the better, are more heterozygous, are in better condition, or
references in Table 1), so we here focus on reviewing the have a better immune response), in some of the best-
current support for the hitherto most widely accepted studied species if anything the opposite effect is found
adaptive explanations. We then highlight several possible [9–11,26]. Only one out of four studies that measured
costs that have received little attention within the prevail- lifetime fitness of offspring (arguably the best measure
ing framework of adaptive thinking. Finally, we outline the of female genetic benefits) found that extra-pair offspring
most plausible models of genetic constraint that could did better [27], whereas in the three other studies, they did
explain how active female extra-pair mating could persist considerably worse [9–11]. A general problem with this
even if it is detrimental to female fitness. approach is that such findings can be confounded by un-
controlled maternal effects (Box 1).
Do females obtain genetic benefits? In sum, the available evidence raises doubts about the
‘Genetic benefit models’ suggest that females obtain either general applicability of the genetic benefits hypothesis
good genes or compatible genes from extra-pair matings, and, despite much work in a variety of socially monoga-
and this idea has been the focus of multiple reviews (e.g., mous species from different taxa, the evidence for in-
[3,5,14–17]). Variants of the genetic benefit hypothesis creased offspring fitness through paternal genetic
have been tested in a variety of species, using one or a contributions remains limited. When looking at the liter-
combination of the following approaches. ature beyond the socially monogamous species, there is
First, the occurrence of extra-pair paternity has been also little support for genetic benefits of mating with
related to variation in adult male traits such as age, several males. A recent meta-analysis [28] of experimental
condition, immune response, and the expression of orna- studies revealed a weak and nonsignificant positive effect
ments. The rationale being that female choice for partly of multiple mating on offspring performance (d = 0.12,
heritable indicators of male viability and fitness provides a P = 0.28, n = 16 species) when excluding other sources of
paternal genetic contribution to offspring survival, attrac- benefits (such as genetic diversity in social insects [29]).
tiveness, or competitive ability. The most generally
reported pattern is that extra-pair sires are older and Do females benefit from fertility insurance?
larger than males that do not sire extra-pair offspring Failed support for the genetic benefit hypothesis has led to
[3,18]. However, it remains controversial whether this is increased popularity of the ‘fertility insurance hypothesis’
necessarily indicative of a good genes benefit [19–21]. [14,30,31]. It has often been taken for granted that extra-
The second approach, used to test the genetic compati- pair mating provides fertility insurance benefits, but a
bility or inbreeding avoidance hypothesis, has been to recent review [30] rightly argues that benefits are obtained
investigate whether extra-pair paternity is more common only under specific circumstances, (e.g., when the partner
when partners are genetically more similar to each other. of the female is truly infertile). However, such male infer-
This pattern has been found in some species (e.g., [22,23]), tility is expected to be a rare phenomenon (because of
making the avoidance of inbreeding a likely adaptive strong selection against infertility), and it is unlikely that
explanation for these cases. Less clear evidence has infertility is detected by females from male indicator traits,
emerged from studies testing whether the genetic similar- such as ornamentation [32,33]. This would mean that,
ity between the female and the extra-pair partner is lower although all females would have to pay the potential costs
than that between the female and her social partner of extra-pair mating, few would obtain a benefit.
(reviewed in [16], but see also [24]). For the latter kind Noticeably, the fertility insurance debate [30] has
of studies, methodological artefacts arising from paternity been centred on possible adaptive explanations for female
assignment probabilities must also be considered [25]. extra-pair mating, while neglecting phenomena that might
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Review Trends in Ecology & Evolution xxx xxxx, Vol. xxx, No. x
Box 1. Do maternal effects confound paternal genetic Box 2. The balance between oligospermy and pathological
effects? polyspermy: a set of hypotheses (H) and tests (T)
The comparison of the fitness of within- and extra-pair offspring H1: sperm numbers on the perivitelline layer (PVL) increase with
from the same brood or litter is the most straightforward test of the numbers of copulations
genetic benefits hypothesis, because many confounding factors that T1: quantify copulations and sperm numbers following [88,89]
also influence fitness can be excluded. Half-siblings that grow up in
the same brood differ in paternal genes or in their level of H2: infertility rates decrease and rates of pathological polyspermy
inbreeding or heterozygosity, but share the same environment, increase with the number of sperm on the PVL (Figure 1, main text)
the same social parents, and the same maternal genes. However, T2: quantify these rates in relation to sperm numbers on the PVL
fitness differences between within- and extra-pair offspring can still following [36,89]
be due to parental effects, for example, if males or females invest
differentially in the two types of offspring. Although this might seem H3: females optimise sperm uptake to maximise hatching success
unlikely [80] and might also lead to the opposite effect that extra- T3: test whether females on average reach their optimum indicated
pair young do worse, recent work provides evidence for an in Figure 1 (main text)
important maternal effect that might lead to higher fitness of
extra-pair young independent of their paternal genotype. H4: infertility rates increase and rates of pathological polyspermy
In many species, early-born or early-hatched offspring outperform decrease when preventing sperm transfer during extra-pair copula-
their later born or hatched brood or littermates. An early start gives tions
them a competitive advantage, which can lead to faster growth, better T4: study reproduction in communal aviaries: enforce monogamy of
condition, and increased chances of survival. Furthermore, in birds, one focal female by fitting all extra-pair males with ‘condoms’
egg content (e.g., resources such as amount of yolk or hormones [81]) (following [90]) and study effects on fertility
often differs depending on the laying sequence, either as a
consequence of changes in female resource availability, or as a result H5: female responsiveness to extra-pair males increases when
of female reproductive decisions, and this also affects offspring rates of within-pair courtship or within-pair copulations or within-
performance ([82]). pair sperm transfer decreases
There is currently no evidence that extra-pair eggs differ from T5: sterilise males, put ‘condoms’ or chemically castrate males
within-pair eggs in size or content, but in some species extra-pair (antiaphrodisiac) and study effects on extra-pair responsiveness
offspring are indeed more common among early laid eggs or early-
hatched offspring ([83–85], but see [86,87]), and controlling for this H6: female responsiveness to extra-pair males increases when
effect reduced the observed difference between extra-pair and experiencing hatching failure
within-pair offspring [83,85]. T6: manipulate hatching success and study extra-pair mating
behaviour following [31].
render extra-pair mating maladaptive. Although mating
with multiple males can insure against infertility and
oligospermy (i.e., a low concentration of sperm) of the social higher than the cost of an egg not getting fertilised. How-
partner [30], it could also increase the risk of embryonic ever, higher sperm numbers should be optimal for males
death and, hence, reduced female fecundity through path- [37,42,43], creating sexual conflict over optimal rates of
ological polyspermy (i.e., fertilisation of an egg by more infertility versus polyspermy. In polyandrous species,
than one sperm) [34–37]. When the DNA of two sperm males are under selection to stack the odds of fertilisation
enters the nucleus of the egg simultaneously, a triploid in their favour by inseminating large numbers of sperm,
embryo can result, which is normally either inviable even if this is partly deleterious to female fecundity [37,43].
[34,36] or sterile [38]. Current knowledge about natural rates of oligospermy and
Extra-pair copulations might increase the risk of path-
ological polyspermy because: (i) these copulations are ad- Female opmum
ditional to within-pair copulations; (ii) extra-pair 1
copulations often transfer greater numbers of sperm than 0.9
Proporon of eggs
0.8
within-pair copulations [39]; and (iii) the partner might
0.7
respond flexibly to a threat of sperm competition by in- 0.6
creasing copulation frequency and potentially ejaculate 0.5
size [40,41]. However, whether extra-pair copulations in- 0.4
crease the risk of polyspermy remains to be shown (Box 2) 0.3
and will depend on patterns of sperm use and storage by 0.2
the female. 0.1
If low sperm numbers increase the risk of eggs not being 0
fertilised whereas high sperm numbers increase the risk of Sperm numbers
pathological polyspermy, then females are selected to take Key: Not ferlised
up, or store, intermediate numbers of sperm, and reject Pathological polyspermy
sperm if there is too much (Figure 1 [37,42]). In egg-laying Surviving embryos
species such as birds, where the cost of laying an infertile TRENDS in Ecology & Evolution
egg should be approximately equal to the cost of laying an
Figure 1. Hypothetical rates of infertility and polyspermy as a function of sperm
egg where the embryo dies of triploidy, the female optimum numbers. The proportion of eggs that fail to be fertilised declines with sperm
is expected to lie where the greatest number of surviving numbers inseminated, whereas the frequency of embryo death due to pathological
embryos is produced (Figure 1). Sperm numbers lower polyspermy increases. The black arrow shows the optimal solution for the female
(maximum of surviving embryos), if the costs of both causes of failure are the
than that should be optimal for female mammals, where same to the female. Note that sperm competition among males will favour males
the cost of aborting a triploid embryo might be (much) that inseminate more sperm than is optimal for the female.
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polyspermy is insufficient to judge whether beneficial or males in the group, if those subordinates can help protect
detrimental effects of multiple mating have the upper hand the offspring against aggression by immigrant males [48].
[37]. We suggest observational and experimental Incidentally, infanticide might also have led to the evolu-
approaches to address this problem (Box 2). tion of social monogamy in mammals, because biparental
A further issue surrounding sperm production illus- care reduces the period during which offspring are vulner-
trates the problem that maladaptive scenarios have re- able to infanticide [49].
ceived insufficient attention. In the germ line, the number In birds, female extra-pair behaviour might also be
of de novo mutations, the majority of which should be associated with the risk of infanticide. Tree swallows
nonbeneficial, increases linearly with the number of cell (Tachycineta bicolor) are one of the most promiscuous
divisions [44]. Therefore, old males and also males with birds: most broods contain extra-pair offspring and the
high levels of sperm production are expected to produce young in a brood are often sired by several extra-pair
sperm carrying more detrimental de novo mutations com- males. Infanticide is not uncommon in tree swallows: if
pared with males whose germ cells have gone through a new male takes over a nest after the female has started
fewer mitotic divisions [19,20,44,45]. Given that successful incubation, the male will wait until the eggs hatch and
extra-pair sires are typically older [18] and might also have then remove the newly hatched offspring, one by one.
higher levels of sperm production, engaging in extra-pair Experimental work showed that if the new male arrived
copulations might be detrimental for females in terms of before the female had finished egg laying, he never com-
inheriting ‘bad genes’ for their offspring. In other words, mitted infanticide, presumably because he copulated with
having a social partner with low levels of sperm production the female [50]. Whether this explains the high level of
can carry a risk of some eggs not getting fertilised, yet the extra-pair paternity is unknown, but it is plausible and
offspring of such males would inherit fewer de novo muta- would also explain why females accept copulations from
tions because their germ cells go through fewer cell divi- many different males, including floaters [51].
sions. Further work is necessary to understand the
likelihood and detriment to female fitness of either of these The genetic constraint argument
scenarios. We do not consider further the roles of male harassment
and forced mating (Box 3), because our review focusses on
Extra-pair mating to avoid infanticide explanations for active female involvement in extra-pair
In species where infanticide occurs, female extra-pair mat- mating. Instead, we now turn to the idea that female extra-
ing might have evolved to avoid infanticide by extra-pair pair behaviour might be maladaptive. Are there species
males. Given the large direct benefits this entails, this where females show active extra-pair mating behaviour
adaptive explanation is rather uncontroversial for those although it is detrimental to them [9–11]? If so, how did
systems where it applies. such behaviour evolve?
In many species, offspring are vulnerable to infanticide
by unrelated males. Such infanticide is adaptive for males
Box 3. Convenience polyandry and harassment
if it increases their chances to mate with the mother of
these offspring. This is often the case, because a female The hypothesis of convenience polyandry [91] states that females
might agree to mate with multiple males only to minimise the costs
that loses her young will enter oestrus sooner (in mam-
arising from male harassment. Although this cannot explain cases
mals) or can lay a replacement clutch (e.g., in birds). where females actively seek extra-pair copulations, convenience
Similarly, in group-living animals, offspring can be vulner- polyandry might be considered as another adaptive explanation for
able to aggression from unrelated males, for example when female extra-pair mating, because reduced resistance by females
competition for essential resources, such as food, shelter, or might minimise the costs of being harassed by males [5]. Although
this hypothesis has received support in a range of studies on
mates, is strong. Even if this does not lead to immediate
promiscuously mating insects [92], more empirical work is needed
death, it can negatively affect offspring fitness. In species to determine whether it is applicable to systems with social
where the risk of infanticide or aggression is high, female monogamy and extra-pair mating, where there might be a capacity
promiscuity might have evolved as an adaptive strategy to for individual recognition. If males can increase the efficiency of their
protect their offspring [46]. This hypothesis predicts that pursuit of extra-pair paternity by strategically allocating their efforts to
those females that have shown low levels of resistance during
any male that has mated with a female will refrain from previous encounters, then females lowering their resistance might
infanticide or aggression, because he might be the father of suffer an increase in the total amount of harassment experienced.
the offspring. Hence, future studies should test the extent to which males
Although the hypothesis has not been tested directly, strategically invest extra-pair mating effort to different females.
there is circumstantial evidence in support. For example, In some species, such as those with intromittent copulatory
organs [93], extra-pair paternity results from forced copulations.
socially polyandrous female bank vole (Myodes glareolus) This is beyond the scope of this review, because there is no active
populations show higher recruitment compared with so- female behaviour that requires further explanation [94]. However, in
cially monandrous populations [47], presumably because of other species, it seems that females actively solicit courtship
reduced infanticide in the former. A review of studies on competition among males [5]. Although the resulting male beha-
viour resembles harassment, females might benefit by selecting the
mammals found that female promiscuity was more com-
most persistent pursuer [95]. However, we note that any benefit of
mon in species in which infanticide occurred (e.g., 62% of 47 such behaviour in terms of producing more persistent sons is
primate species) than in species where infanticide was included in the fitness measures of some of the empirical studies
unlikely (9% of 11 primate species) [46]. testing ‘genetic benefit models’ mentioned above, although no
An interesting twist to the story is that dominant males study in such a system has measured differences in sexual
behaviour among offspring.
might even ‘encourage’ female mating with subordinate
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Intersexual pleiotropy Intrasexual pleiotropy Box 4. The parallel debate about female orgasm
Following Lloyd’s controversial book on female orgasm in humans
Polymorphic genes Polymorphic genes
[96], there has been a lively debate about whether female orgasm
with pleiotropic with pleiotropic evolved as a by-product of strong selection on the male orgasm and
effects effects
Measurable
as genec ejaculation system [97] or serves adaptive functions of its own (e.g.,
correlaons pair-bond hypothesis or sire choice hypothesis, reviewed in [67]). A
recent quantitative genetic study on male and female orgasmic
Female extra- function in humans found no significant between-sex genetic
Male extra-pair Female
pair mang
mang success
behaviour
ferlity correlation [97–99], providing no support for the idea that female
orgasm exists as an epiphenomenon of male orgasm.
Measurable in
However, the absence of a between-sex genetic correlation does
knockout or
Monomorphic Monomorphic knockdown not disprove the by-product hypothesis. It is possible that persistent
genes with genes with experiments selection on male orgasmic function keeps the genes involved in a
pleiotropic funcon pleiotropic funcon monomorphic state (i.e., novel alleles associated with reduced
orgasmic function are always driven to extinction). Given that only
TRENDS in Ecology & Evolution polymorphic loci contribute to genetic variance (and, hence,
possible covariance between the sexes), the effect of these
Figure 2. Pleiotropic gene effects and the existence of female extra-pair mating monomorphic genes cannot be quantified, although these genes
behaviour. Illustration of how the concepts of intra- and intersexual pleiotropy can still might be responsible for why females experience orgasms [67].
explain the existence of female extra-pair mating behaviour as genetic corollaries
Only experiments where a certain gene is knocked out or its
of either male extra-pair mating success or female fertility.
translation reduced by RNA interference might reveal such under-
lying pleiotropy (Figure 2, main text).
Genetic constraint models for extra-pair mating propose Equally problematically, if a positive genetic correlation between
the sexes is found, this does not imply that the trait in one sex
that the alleles that cause maladaptive female promiscuity
evolved only due to correlated selection on the trait in the other sex.
have additional pleiotropic effects that are beneficial and, Hence, female orgasm might or might not serve an adaptive
hence, maintain the alleles in the population. To test this function irrespective of its genetic architecture.
idea, we need to identify the beneficial side effects of such
alleles. Note that this does not require knowing the specific
alleles that affect female extra-pair mating. The genetic bond by modifying this molecular machinery shared
constraint of interest can be studied by estimating genetic between the sexes might then create similar effects in both
correlations between female extra-pair mating propensity sexes. Hence, in species where extra-pair mating is
and other traits that we suspect to be affected by the same primarily a question of the strength of the pair bond, a
genes. In the following, we distinguish between two cases, positive genetic correlation between female and male ex-
depending on whether these other traits are expressed by tra-pair mating propensity might be expected.
the other sex (i.e., in males; intersexual pleiotropy) or by The between-sex genetic correlation (rMF) for female
the same sex (i.e., in females; intrasexual pleiotropy). and male extra-pair mating has recently been estimated
in a captive population of a pair-bonding species, the zebra
Intersexual antagonistic pleiotropy finch (Taeniopygia guttata) [12]. The obtained value of
The hypothesis of ‘intersexual antagonistic pleiotropy’ rMF=0.6 suggests that a substantial proportion of the
refers to genes that have pleiotropic effects on the two sexes, additive genetic variance for male extra-pair mating suc-
such that they enhance fitness in one sex, while reducing it cess has pleiotropic effects on female extra-pair mating
in the other. Here, the hypothesis argues that nonadaptive propensity, such that the latter could evolve largely as a by-
female extra-pair mating is caused by alleles under strong product of strong selection on the former. Such a strong
positive selection in males, because they enhance male genetic correlation argues for between-sex pleiotropy, be-
extra-pair paternity gains (Figure 2). In other words, female cause linkage disequilibrium caused by assortative mating
and male promiscuity might be homologous traits that are between promiscuous males and females should at best
influenced by the same set of genes, with alleles contributing produce a weak positive correlation. This is because assor-
to male extra-pair mating success and also facilitating tative mating is far from complete (due to the many within-
female extra-pair behaviour (note that a similar argument pair young) and because the heritability of the level of
has been made to explain female orgasm; Box 4). extra-pair mating that leads to extra-pair paternity is
When this hypothesis was proposed for multiple mating small [12,53,54]. However, only a selection experiment
in general (rather than for extra-pair mating specifically) that tries to decouple male from female promiscuity could
in a short commentary in 1987 [6], the hypothesis was fully reveal the degree of pleiotropy.
rapidly criticised as unrealistic [8]. The main criticism was Strong positive estimates of rMF might be the default, if
that female and male promiscuity are unlikely to be ho- the focal traits are homologous. A meta-analysis [55] found
mologous traits, because the mating behaviours of the two a mean rMF=0.77 for behavioural traits, which is not
sexes are often different. This might be valid for species different from that for morphological traits (rMF=0.80).
where males and females indeed take different roles in Somewhat lower genetic between-sex correlations might
mating and do not form pair bonds. However, in socially be expected for traits that are strongly sexually dimorphic
monogamous species, the behavioural repertoire of both (see Figure 4 in [55]). This calls for caution, because the
sexes is often more similar. If pair bonding evolves de novo, propensity to engage in extra-pair mating is probably
it is likely to evolve simultaneously in the two sexes based higher in males than in females of most species (e.g.,
on the same molecular mechanisms (but see, e.g., [52]). Any [56,57]). This observation might also be interpreted as
genetic mutation that strengthens or weakens the pair the result of past antagonistic selection on the expression
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0.4 variation, as evidenced by high estimates of the heritabili-
Key: Extraversion
ty of this variation [59,60]. At the other extreme, field
Agreeableness studies of birds that are limited to quantifying the realised
Conscienousness amount of extra-pair paternity (rather than the underlying
Neurocism
propensity, or engagement in extra-pair copulations, which
0.2
Openness
in itself is rarely quantified) have found low heritability
estimates [53,54]. This is expected, because paternity
Male correlaon
(from the female perspective) will additionally depend
on the mating opportunities of a female, mate guarding
0.0
by her partner, sperm competition and other postcopula-
tory processes. Hence, extra-pair paternity in a brood will
only partly reflect the underlying propensity of a female to
engage in extra-pair matings. Likewise, the extra-pair
–0.2
N = 211 mating success of a male might strongly depend on the
mating preferences of the available females and only to
N = 3525 some extent on his extra-pair mating effort (his intrinsic
–0.4
propensity). Studies in captivity have the advantage that
–0.4 –0.2 0.0 0.2 0.4
behavioural propensities such as the responsiveness of a
Female correlaon female to extra-pair courtship or the extra-pair mating
TRENDS in Ecology & Evolution effort of a male can be measured directly. Higher herit-
abilities of these measures [12] will enable estimation of
Figure 3. Phenotypic correlates of extra-pair mating behaviour in humans are
shared between the sexes. The scatterplot shows male and female correlation
between-sex genetic correlations with smaller amounts of
coefficients between infidelity (lack of relation exclusivity) and the Big Five error.
personality traits across ten different regions of the world: (1) North America (N = Despite the difficulty of measuring rMF in the wild,
3525); (2) South America (N = 622); (3) Western Europe (N = 2269); (4) Eastern
Europe (N = 1923); (5) Southern Europe (N = 1074); (6) Middle East (N = 885); (7)
it might be worth testing whether male relatives (e.g.,
Africa (N = 800); (8) Oceania (N = 804); (9) South and Southeast Asia (N = 211); and brothers) of females that have extra-pair offspring have
(10) East Asia (N = 1075). N represents the sum of male and female sample sizes. a higher fitness through extra-pair paternity compared
Data from [100].
with male relatives of faithful females.
Intersexual antagonistic pleiotropy could be considered
of promiscuous behaviour in the two sexes, moving them a form of indirect selection, where all the male carriers of
further apart and bringing them closer to their sex-specific an allele for promiscuity make up for the lower fitness of
optima (monogamy for females and promiscuity for males). the female carriers. Note that this is different from indirect
Although rMF has not been estimated for extra-pair selection through ‘sexy son’ benefits [61,62], where the
mating propensity in humans, numerous studies have promiscuous behaviour of the female per se increases
focussed on describing phenotypic correlates (e.g., person- the attractiveness and, hence, fitness of her sons (leading
ality traits) related to this propensity (Figure 3). It is to more grandchildren) via a paternal genetic effect. Under
noteworthy that these correlates go in the same direction sexually antagonistic pleiotropy, when an evolutionary
for males and females, suggesting that much of this beha- equilibrium is reached, the ‘promiscuous son benefit’
vioural syndrome is shared between the sexes. It is (adaptive promiscuous behaviour by males) will be com-
also plausible that these correlated traits show positive pensated by a ‘promiscuous daughter cost’ (maladaptive
between-sex genetic correlations, such that, for instance, promiscuous behaviour by females). Furthermore, the sce-
risk-taking fathers will tend to sire risk-taking daughters. nario allows for the female behaviour to be truly maladap-
A frequently used argument is that strong antagonistic tive (due to costs listed in Table 1 leading to fewer
selection will promote the evolution of sex-specific regula- grandchildren).
tion of the underlying genes (leading to sexual dimorphism
and possibly reducing rMF). However, complex quantitative Intrasexual antagonistic pleiotropy
genetic traits such as personality are likely to depend on The hypothesis of ‘intrasexual antagonistic pleiotropy’
hundreds of genes [58], such that a complete sex-specific argues that alleles for female extra-pair mating are main-
regulation of allelic effects at all these loci will be difficult, tained because these alleles have pleiotropic effects on
if not impossible, to achieve. The example of human infi- female fecundity (Figure 2) or on female behaviours that
delity (Figure 3) is particularly striking in that respect. A are under positive selection, such as receptivity towards
vast number of genes are likely to affect each personality the social mate [4,12], the ability to divorce, or novelty-
component that will, in turn, influence the probability of seeking behaviour [63].
engaging in extra-pair mating. However, once such a ge- A review on the costs and benefits of female extra-pair
netic correlation is in place, selection will favour females mating behaviour [4] suggested that alleles for female
that ‘make the best of a bad job’, for instance by becoming resistance towards extra-pair males do not spread in a
more choosy and seeking good-gene benefits. population because these alleles also induce female resis-
The largest handicap for measuring rMF is the difficulty tance towards their partners, thereby leading to infertility
in obtaining good measures of an individual’s propensity to and reduced fitness. This idea of a genetic correlation
engage in extra-pair mating. At the one extreme lie human between female extra-pair and within-pair responsiveness
questionnaire studies that seem capable of capturing this has been tested and tentatively rejected for captive zebra
6
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Review Trends in Ecology & Evolution xxx xxxx, Vol. xxx, No. x
finches [12], yet the hypothesis deserves further examina- observations, standardised personality tests, and experi-
tion, especially in species that form weaker and more mental manipulations.
ephemeral pair bonds. Although studies of genetic correlations can check the
Copulation frequency could evolve as a genetic corollary plausibility of constraint arguments, long-term studies of
of female fecundity [64], because copulations might be fitness consequences from the wild are needed to assess
proximately linked to stimulating reproductive processes whether and under what circumstances female extra-pair
[65,66]. Likewise, the degree of female sexual arousal behaviour is adaptive or maladaptive.
might evolve with female fertility, if arousal serves the
function of enhancing sperm uptake ([67], but see the issue Acknowledgements
of polyspermy discussed above). Under these scenarios, We thank Yu-Hsun Hsu, Malika Ihle, Emmi Schlicht, and two
female extra-pair mating could evolve as a by-product anonymous reviewers for constructive comments on the manuscript,
and the Alexander von Humboldt Foundation (travel grants) and the Max
of selection on fertility via an increased propensity to Planck Society for support.
copulate.
Extra-pair mating behaviour might also result from a
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