# Sexual Conflict Arising from Extrapair Matings in Birds

Alexis S Chaine, Robert Montgomerie, Bruce E Lyon

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Alexis S Chaine, Robert Montgomerie, Bruce E Lyon. Sexual Conflict Arising from Extrapair Matings in Birds. Cold Spring Harbor Perspectives in Biology, 2015, 7 (3), pp.a017590. 10.1101/cshperspect.a017590. hal-04967723

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Distributed under a Creative Commons Attribution 4.0 International License
Sexual Conflict Arising from Extrapair
Matings in Birds

Alexis S. Chaine<fnref n="1" />, Robert Montgomerie<fnref n="2" />, and Bruce E. Lyon<fnref n="3" />

*Correspondence*: lyon@biology.ucsc.edu

The discovery that extrapair copulation (EPC) and extrapair paternity (EPP) are common in birds led to a paradigm shift in our understanding of the evolution of mating systems. The prevalence of extrapair matings in pair-bonded species sets the stage for sexual conflict, and a recent focus has been to consider how this conflict can shape variation in extrapair mating rates. Here, we invert the causal arrow and consider the consequences of extrapair matings for sexual conflict. Extrapair matings shift sexual conflict from a simple two-player (male vs. female) game to a game with three or more players, the nature of which we illustrate with simple diagrams that highlight the net costs and benefits of extrapair matings to each player. This approach helps identify the sorts of traits that might be under selection because of sexual conflict. Whether EPP is driven primarily by the extrapair male or the within-pair female profoundly influences which players are in conflict, but the overall pattern of conflict varies little among different mating systems. Different aspects of conflict are manifest at different stages of the breeding cycle and can be profitably considered as distinct episodes of selection caused by conflict. This perspective is illuminating both because conflict between specific players can change across episodes and because the traits that evolve to mediate conflict likely differ between episodes. Although EPP clearly leads to sexual conflict, we suggest that the link between sexual conflict and multiple paternity might be usefully understood by examining how deviations from lifetime sexual monogamy influence sexual conflict.

The development of genetic tools for deter-
mining parentage fundamentally altered our
understanding of animal mating systems (Jef-
freys et al. 1985; Avise 1996; Reynolds 1996)
and provided invaluable insights into the con-
sequences and causes of females mating with
more than one male. Particularly for the study
of birds, these methods revealed that social pair
bonds often fail to match the actual patterns of

copulations that produced offspring (Gowaty
and Karlin 1984; Birkhead and Møller 1992;
Reynolds 1996; Petrie and Kempenaers 1998),
revolutionizing the study of avian mating sys-
tems. Extensive research and two recent reviews
point out the progress we have made in this
field and show how little we still understand
extrapair behavior (Griffith et al. 2002; West-
neat and Stewart 2003).

<footnote n="1">¹Station d'Écologie Expérimentale du Centre National de la Recherche Scientifique (CNRS), 09200 Moulis, France</footnote>

<footnote n="2">²Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada</footnote>

<footnote n="3">³Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064</footnote>
A.S. Chaine et al.

In the 1960s, David Lack compiled what was then known about mating systems in birds and concluded that >90% of species were monogamous, a pattern that provided an early framework for the development of mating system theory (Lack 1968; Orians 1969; Emlen and Oring 1977). When it was later discovered that sexual mating patterns did not match the social mating systems that Lack described, the field was turned on its head (Westneat et al. 1990; Avise 1996; Reynolds 1996; Zeh and Zeh 2001). In extreme cases, the mismatch between the social and sexual mating systems is nothing short of spectacular; in fairywrens (*Malurus* species) that are socially monogamous, cooperatively breeding species with helpers, the extrapair paternity (EPP) rate can exceed 75% of all offspring and 95% of all broods (Mulder et al. 1994). In socially monogamous birds, in general, the rate of EPP is typically on the order of 10% of offspring and 20% of broods (Griffith et al. 2002), but variation among species, and even populations within species, is extensive (Arnold and Owens 2002; Griffith et al. 2002). The occurrence of EPP has profound consequences for the evolution of social behavior, both because it alters the scope for the action of sexual selection (Webster et al. 1995; Sheldon and Ellegren 1999) and because it results in males often providing parental care to offspring they have not sired (Davies et al. 1992; Westneat and Sherman 1993).

Even in taxa with mating systems other than social monogamy, or in which there is no obvious pair bond, the ability to determine parentage genetically was revolutionary, allowing precise estimates of male reproductive success when females mate multiply. That focus on multiple mating also catalyzed an interest in sexual selection from the female's perspective, whereas previous attention had been strongly biased toward males and male traits. More specifically, it raised the questions as to why females would pursue and benefit from matings outside the social pair bond (Westneat et al. 1990; Petrie and Kempenaers 1998), and why a female would benefit from mating with more than one male for a given clutch or litter. This new focus on females brought attention to the issue of polyandry more generally (Jennions and Petrie

2000; Simmons 2005; Parker and Birkhead 2013; Pizzari and Wedell 2013).

Recently, the assumption that females control mating patterns, and thus that polyandry and EPP can be universally understood from the perspective of fitness benefits to females, has been questioned (Westneat and Stewart 2003). Focusing specifically on EPP, Westneat and Stewart (2003) suggested that, in some taxa, EPP could be driven entirely by benefits to the extrapair-seeking male. They also suggested that many aspects of EPP can be profitably explored from the perspective of sexual conflict, as had Petrie and Kempenaers (1998) before them. Previous interest in the relation between EPP and sexual conflict in birds was focused particularly on trying to explain the incidence and frequency of EPP within and among species. Westneat and Stewart (2003) recognized that that link was indirect. Instead, they suggested that sexual conflict theory might help us to identify traits that could arise from conflict and that those traits might inform the search for a general explanation of the huge variation in EPP rates both among and within bird species.

Sexual conflict, the conflicting fitness interests of males and females during mating (Parker 1979; Rice 1998; Arnqvist and Rowe 2005), can lead to antagonistic coevolution between the traits expressed in males and those expressed in females, traits that in some way influence mating outcomes. Traits in males and females are ultimately the drivers of conflict, and, reciprocally, conflict fuels further trait evolution. Sexual conflict theory is useful because it can potentially explain the evolution and maintenance of traits that are otherwise difficult to understand (Arnqvist and Rowe 2005). Thus, studies often examine the factors and traits that underlie different aspects of sexual conflict, as well as the types of morphological and behavioral traits that result from selection caused by the sexual conflict itself.

In this article, we build on the foundation provided by Westneat and Stewart (2003). They proposed that sexual conflict can help to explain variation in the occurrence of EPP among species and populations (Westneat and Stewart 2003). Here, we invert the focus and seek
Sexual Conflict from Extrapair Matings in Birds

to understand the consequences that EPP can
have for sexual conflict and the relation between
EPP and other drivers of sexual conflict. Thus,
we examine the players involved in the sexual
conflict generated by EPP and the costs and
benefits that underpin the conflicts among the
different players. We point out that different
conflicts are involved in the different stages of
a single bout of reproduction, and we suggest
that these represent sequential periods of con-
flict, each of which is a different episode of se-
lection generated from that conflict. We then
place these patterns of conflict into a broader
context by contrasting how different patterns of
fidelity and infidelity (including EPP) during a
lifetime of mating can influence sexual conflict.
Our review focuses on birds as examples, both
because they have been extensively studied with
respect to EPP and because they have been the
subjects of most of our own research. Our goal,
however, is to provide a framework for under-
standing trait evolution under the influence of
sexual conflict caused by females mating multi-
ply in any animal species.

THE PLAYERS

Sexual conflict is often seen as a conflict between
males and females. However, when females mate
with more than one male, sexual conflict nec-
essarily becomes a multiplayer game. The play-
ers include at least the pair female, pair male,
and extrapair male (Petrie and Kempenears
1998; Rice 1998; Westneat and Stewart 2003;
Alonzo and Pizzari 2013). In some cases, the
female paired with the extrapair male may also
suffer fitness losses because of her mate's activ-
ities, in which case, the conflict becomes a four-
player game (Petrie and Kempenaers 1998). In-
deed, in specific cases, more than four players
may also be involved if, for example, there are
multiple extrapair males, multiple females are
affected by the extrapair behavior in a polygy-
nous system, or EPP affects the fitness of
nonbreeding individuals, such as helpers in co-
operative breeders.

The complexities involved in the sorts of
conflicts generated by EPP can be usefully illus-
trated with conflict-of-interest diagrams that

show all of the players involved (Fig. 1; see
also Petrie and Kempenaers 1998; Rice 1998).
For example, the addition of an extrapair male
to the simple conflict between the sexes in a
mated pair potentially creates two sexual con-
flicts—one between the female and her mate
and the other between the same female and
the extrapair male—as well as intrasexual con-
flict between the two males (Fig. 1). The dy-
namics of the conflict between any two of these
players can be affected by the other conflicts
of interests in the triad (Westneat and Stewart
2003). Thus, to fully understand how sexual
conflict affects trait evolution, we need to con-
sider all conflict interactions, including how
intrasexual conflict between males influences

<figure><img src="image_2.png" /><figcaption>Female-driven EPP</figcaption></figure>

<figure><img src="image_3.png" /><figcaption>Male-driven EPP</figcaption></figure>

<figure><img src="image_4.png" /></figure>

**Figure 1.** Conflicts of interests between males and females over the occurrence of extrapair matings in socially monogamous mating systems. Symbols for extrapair males are solid black. Red bars join individuals that are in conflict over the occurrence of extra-pair matings, whereas blue bars join individuals that agree on the optimal level (zero for male-driven) of extrapair mating. Two different socially monogamous systems are shown here: (A) When females benefit from EPP (i.e., EPP is female driven), the female and EPP male both benefit from EPP and are in conflict with the within-pair male (e.g., American robin *Turdus migratorius*), and (B) when EPP is solely driven by the fitness interests of the extrapair male (i.e., EPP is male driven), both the female and within-pair male are in conflict with the extrapair male (e.g., lark bunting *Calamospiza melanocorys* shown here with a male attempting an EPC while the pair male tries to fend him off). (Both photos courtesy of B. Lyon.)
A.S. Chaine et al.

conflict between the sexes. It is important to
recognize that extrapair matings generate dif-
ferent conflicts that manifest themselves at suc-
cessive stages of reproduction (e.g., conflict over
mating, fertilization, and postfertilization in-
vestment; see the section Episodes of Conflict
over EPP: When and over What?). In this first
section, we use conflict-of-interest diagrams
to focus only on the conflict over the occurrence
of extrapair copulations (EPCs) and not dur-
ing the subsequent episodes of reproduction.
We provide details on only one stage of repro-
duction because the basic nature of the conflict
can change across episodes (see below), and

hence a single diagram is often specific to one
episode.

Our conflict-of-interest diagrams (Fig. 1) illustrate simply whether or not there is conflict between two players; we ignore the strength of the conflict and avoid assumptions about which player causes the conflict, hence the lack of arrows denoting a direction of conflict. Blue links indicate when two players both share the same optimal level (zero for male-driven) of extrapair mating, red links denote conflicts of interest over the occurrence of that mating, and, in Figure 2, thin black lines denote pairs of socially interacting individuals whose joint fitness inter-

<figure><img src="image_5.png" /><figcaption>**Figure 2.** Conflicts of interests between focal males and females in relation to breeding system. Symbols for extrapair males and their social mates in solid black. Red bars join individuals that are in conflict over the occurrence of the extrapair matings, whereas blue bars join individuals that share the same optimal level (zero for male-driven) or extrapair mating; thin black lines indicate no particular costs or benefits. All cases shown involve female-driven EPP, in which the female benefits from the extrapair mating. Photos show one example species of each mating system: (A) Tree swallow (*Tachycineta bicolor*), (B) purple martin (*Progne subis*), (C) red-winged blackbird (*Agelaius phoeniceus*), (D) Smith's longspur (*Calcarius pictus*), (E) red phalarope, and (F) splendid fairywren (*Malurus splendens*). (All photos courtesy of B. Lyon, except Smith's longspur, which is provided by Ian Davies.)</figcaption></figure>
ests are not affected by the extrapair mating. The
two males will typically be in conflict over the
occurrence of the EPCs because they compete
to fertilize the same ova—usually a zero-sum
game. Although male-male cooperation over
matings with a single female is theoretically fea-
sible (e.g., when courtship and copulation with
different males greatly stimulate female fecun-
dity [Alonzo and Pizzari 2013]), this idea re-
mains to be tested empirically.

These conflict-of-interest diagrams help to illustrate how conflict changes under different social scenarios. A fundamental debate, for example, is whether or not EPP benefits females (Mulder et al. 1994; Westneat and Stewart 2003; Arnqvist and Kirkpatrick 2005; Griffith 2007; Dunn et al. 2013). The sex that promotes the occurrence of an extrapair mating also critically influences the pattern of sexual conflict over such matings: Male- and female-driven EPP result in opposite patterns of conflict over whether extrapair matings should occur (Petrie and Kempenears 1998) and hence opposite patterns of selection on traits (Fig. 1A,B). Importantly, sexual conflict over EPP occurs whether it is male or female driven; what changes is whether the conflict is within the pair or between the extrapair male and both members of the pair (Fig. 1A,B).

In socially monogamous species with fe-
male-driven EPP, the female and extrapair
male share a benefit from EPP, whereas the fe-
male and her mate are in conflict over the oc-
currence of the EPC (Fig. 1A). Thus, we ex-
pect to see traits that enhance the extrapair
male's ability to court the female, the pair male's
ability to guard his mate, and the female's abil-
ity to evade mate guarding and thereby sneak
away to copulate with an extrapair male. Mate
guarding by the within-pair male appears to
be particularly widespread (Møller and Birk-
head 1991; Kokko and Morrell 2005; Pedersen
et al. 2006), but there is also some evidence
that the extrapair male and pair female use tac-
tics to enhance their copulation success. Superb
fairywren (Malurus cyaneus) females, for exam-
ple, go on extrapair forays to seek EPCs before
dawn (Double and Cockburn 2000), presum-
ably to avoid detection by their social mate.

Intriguingly, male fairywrens seek EPCs with a unique display behavior—a flower petal display—that they use only when courting females seeking EPCs (Mulder 1997; Karubian and Alvarado 2003). Alternatively, Dunnock (*Prunella modularis*) females fly quickly to try to “lose” their social mate when they are seeking extrapair mates, and copulations with those extrapair males are exceptionally rapid and cryptic (Davies 1992). Females may also adopt countertactics to incite male-male competition and thereby thwart tenacious mate guarding by their mates (Montgomerie and Thornhill 1989); female bearded seedlings (*Panurus biarmicus*), for example, produce a call that attracts the attention of multiple extrapair males and this has been interpreted as a means for the female to increase the frequency of EPCs (Hoi 1997).

When EPP is driven by extrapair males, the female and her mate might both benefit from preventing EPCs, and thus both would be in conflict with an extrapair male (Fig. 1B). In this situation, we expect evidence for forced or coerced copulations by the extrapair male and cooperation between the pair members to prevent them. Females, for example, might call to attract the attention of their mate when an extrapair male approaches in pursuit of copulations. There are no clear avian examples of such tactics, but female moose (*Alces alces*) call to attract the attention of the dominant male when subordinate males attempt to force copulations (Bowyer et al. 2011). Extrapair males, on the other hand, should evolve morphologies or behaviors to force matings that females are trying to avoid. Thus, cloacal protuberances in male birds may have been favored specifically because of benefits they provide in securing EPP, as they occur most commonly in species in which there is sperm competition because of extrapair matings (Briskie 1993; Tuttle et al. 1996). A few taxa of birds, particularly waterfowl and ratites, also have penises and these structures may have evolved particularly to help extrapair males overcome female defenses (Briskie and Montgomerie 1997; Brennan et al. 2007).

Variation in breeding system (i.e., in pat-
terns of association between the sexes and
parentage) might be expected to impact how
A.S. Chaine et al.

EPP influences sexual conflict because different
breeding systems vary in the numbers of socially
interacting individuals. It is therefore surprising
that the overall patterns of conflict over the oc-
currence of extrapair matings would appear to be
similar across breeding systems (Fig. 2A–F). On
reflection, this makes sense because EPP is about
the sexual (genetic) patterns of reproduction,
and these are actually quite similar across social
systems. The patterns of conflict only differ when
EPP influences either the social patterns or pa-
rental care trade-offs among more than one male
and female, such as in social polygyny andry (Fig.
2D), when males provision offspring at more
than one nest (Davies 1992; Briskie et al. 1998).
Likewise, social polyandry can lead to mixed pa-
tternity in one or more clutches (Fig. 2E), either
because females mate simultaneously with mul-
tiple males or because sperm from a first re-
productive bout can be stored and sire offspring
from a second clutch, a pattern documented for
role-reversed species like spotted sandpipers
(*Actitis macularius* [Oring et al. 1992] or red
phalaropes (*Phalaropus fulicarius* [Dale et al.
1999]). Although these conflict patterns resem-
ble the basic interactions in social monogamy,
a key difference in polygamous and polyan-
drous breeding systems is that all of the males
are socially paired with the same female, and
the conflict thus comes from within the breeding
association, not from outside.

In one other breeding system, cooperative
breeding, the pattern of sexual conflict among
breeding adults is similar to that in social mo-
nogamy, but the occurrence of EPP has a special
influence on other social group members, the
 helpers (Fig. 2F). The presence of extrapair off-
spring in the brood reduces the relatedness
between helpers and the offspring they are help-
ing to raise, thus reducing the indirect benefits
from helping (Charnov 1981). This creates con-
flict between helpers and their mother, which,
in turn, should favor helpers that discourage
the occurrence of extrapair matings. How co-
operative breeding remains stable under the ex-
tremely high levels of EPP observed in some
fairywrens (Malurus species) is puzzling. Possi-
bly, females show very high fidelity to the same
extrapair male across years, in which case, help-

ers would often be assisting their mother to
raise full siblings.

BENEFITS AND COSTS OF EPP AS DRIVERS
OF CONFLICT

Sexual conflict occurs because the fitness in-
terests of the sexes can differ during the vari-
ous stages of reproduction. Thus, to understand
how and why EPP generates sexual conflict, and
how this source of conflict compares with other
forms of sexual conflict, we need to understand
the costs and benefits of the extrapair matings to
the different players.

The benefits that males gain from extrapair
matings have long been clear (Trivers 1972): via
EPP, males sire more offspring than would oth-
erwise be possible. Any benefits gained by the
extrapair male are thought to lead to direct fit-
ness costs for the within-pair male because the
within-pair male then sires fewer offspring than
he would otherwise. But EPP may cause females
to increase their investment, either through
the stimulatory effects of ejaculates from mul-
tiple males (Alonzo and Pizzari 2013) or when
females engage in EPP to upgrade the genetic
quality of their offspring, resulting in differen-
tial allocation of maternal care (Burley 1988).
Thus, changes in female investment should be
considered when evaluating the fitness costs to
the pair male and the effects on his contribution
to parental care (Sheldon 2000, 2002).

For females, extrapair matings potentially
bring a wide variety of direct and indirect fitness
benefits, but the importance of indirect bene-
fits remains controversial (Arnqvist and Kirk-
patrick 2005; Griffith 2007). Direct benefits
of EPC can accrue from an increase in the num-
ber of fertilized ova (e.g., when the pair male is
infertile or has limited sperm available [Sheldon
1994]), access to more resources (e.g., extrapair
male's territory or paternal care [Davies 1992;
Briskie et al. 1998]), and a reduction in harass-
ment by those males seeking EPCs (Rowe 1992;
Gowaty and Buschhaus 1997). In species with
sexually selected infanticide by males, females
that mate multiply (via polyandry or EPP)
might reduce the risk of infanticide of their
eggs or offspring if infanticide is performed by
males that have not copulated with the female (Agrell et al. 1998; Soltis et al. 2000). Potential indirect benefits include the genetic benefits that accrue from an increase in the quality, rather than quantity, of offspring (good genes in a viability or sexual context [Slayter et al. 2012; Madsen et al 1992] or genetic complementarity [Zeh and Zeh 2006]), an increase in the genetic diversity of offspring (Slayter et al. 2012; Parker and Birkhead 2013), or a reduction of inbreeding depression when females are socially paired with a relative (Blomqvist et al. 2002; Cornell and Tregenza 2007). Note that these female benefits are identical to benefits from polyandry generally (i.e., when females mate with more than one male during a reproductive bout [Schlicht and Kempenaers 2011; Slayter et al. 2012; Parker and Birkhead 2013]).

There are also likely to be fitness costs to fe-
males from extrapair matings, especially when
EPP is driven solely by the fitness interests of the
extrapair male, such as when the copulations are
forced or coerced (Westneat and Stewart 2003).
In addition to the risk of injury or transfer of
sexually transmitted diseases during mating,
the female suffers a potential indirect loss of fit-
ness by having some of her offspring sired by a
nonpreferred male—a cost that is the inverse of
the benefits a female gains when EPP is female
driven. Females may also suffer a cost due to the
loss of parental care from her social mate when
he suspects EPP (Sheldon 2002; Griffin et al.
2013). Finally, there are also potential costs to
the female mated to a male who seeks EPCs—
his extrapair matings could increase her risk
of contracting sexually transmitted diseases or
could result in lower investment from her mate
if he invests time seeking extrapair mates (Ma-
grath and Elgar 1997; Magrath and Komdeur
2003). In theory, the extrapair male's mate could
also suffer fitness losses if the extrapair male
allows the other female to access his territorial
resources or if he provides food to her offspring.

EPISODES OF CONFLICT OVER EPP—WHEN
AND OVER WHAT?

In their broad survey of the natural history of
sexual conflict, Arnqvist and Rowe (2005) noted

that sexual conflict can occur during any inter-
action between a male and female, not just when
deciding whom to mate with. They identified
three main types of interactions as the “com-
ponents” of conflict: (1) conflict before copu-
lation, (2) conflict during the period from cop-
ulation to fertilization of the zygote, and (3)
conflict after fertilization, over parental invest-
ment. We suggest that these three components
delineate clear episodes of selection because
they are temporally distinct bouts that connect
in a temporal sequence to influence lifetime
fitness (Arnold and Wade 1984; Moore 1990;
McGlothlin 2010). Thinking about episodes of
selection helps clarify how these different peri-
ods of conflict are linked through their effects on
fitness, how selection driven by conflict might
be resolved, and how different types of traits are
often favored during the different episodes.

The different episodes of conflict differ in
some critical ways with respect to EPP. First, the
basic nature of the conflict can invert from one
episode to the next. For example, with male-
driven EPP, the female and her mate should
cooperate to prevent extrapair mating attempts,
but when an EPC does occur and is detected by
the pair male, it can trigger conflict between the
paired male and female over postfertilization
investment. Males should not invest in offspring
they have not sired whether that EPP was male
or female driven. Second, the traits that mediate
conflict (i.e., that evolve in response to conflict)
differ across the episodes, both in the types of
traits and in the degree to which they show can-
alization or plasticity among mating roles. The
same traits that mediate conflict over the deci-
sion to mate are not likely to be the same as
those that mediate fertilization success or pa-
rental investment.

Likewise, plastic traits are probably more
useful in some episodes than in others. Traits
shows plasticity when their expression depends
on the mating role in which they are manifest
(e.g., different expression in extrapair versus
within-pair males) (Fig. 1) (Petrie and Kempe-
naers 1998; Ball and Parker 2003; Westneat and
Stewart 2003; Parker 2006; Alonzo and Pizzari
2013). Role-specific traits must necessarily be
flexible, and they also require an assessment
A.S. Chaine et al.

mechanism that can link trait expression to its
specific role. Behavioral traits provide the sim-
plest way to achieve role flexibility. Thus, plas-
ticity may be more likely in episodes in which
behavior is important (e.g., premating deci-
sions and parental care), whereas canalized
traits may be more likely when physiology, rath-
er than behavior, is the mediator of conflict
(e.g., fertilization success).

Before copulation, there is sexual conflict
that favors traits in the extrapair male that in-
crease the success of his extrapair mating at-
tempts, in the within-pair male that decrease
the copulation success of the extrapair male,
and in the females that enhance or decrease
the success of extrapair matings, depending on
whether or not the female benefits from those
matings. Because the premating episode mainly
involves behavioral interactions between indi-
viduals, there is much potential for role-specific
trait expression and ample evidence for differ-
ences in the behaviors of the extrapair and with-
in-pair males (e.g., territorial vs. sneaker males).
Once an EPC occurs, the conflict shifts to
interactions that influence fertilization success
within the female's reproductive tract. Sperm
number and characteristics as well as ejaculate
properties mediate that conflict for males,
whereas sperm storage structures and reproduc-
tive tract secretions play a role in mediating the
conflict over fertilization success for females
(Birkhead et al. 1993; Briskie and Montgomerie
1993). Males thus have the opportunity to ad-
just sperm number or ejaculate size specifical-
ly in the context of pursuing EPP (Parker 1990;
Birkhead and Fletcher 1992; Birkhead et al.
1995; Pizzari et al. 2003).

Once an EPC occurs, the conflict shifts to
interactions that influence fertilization success
within the female's reproductive tract. Sperm
number and characteristics as well as ejaculate
properties mediate that conflict for males,
whereas sperm storage structures and reproduc-
tive tract secretions play a role in mediating the
conflict over fertilization success for females
(Birkhead et al. 1993; Briskie and Montgomerie
1993). Males thus have the opportunity to ad-
just sperm number or ejaculate size specifical-
ly in the context of pursuing EPP (Parker 1990;
Birkhead and Fletcher 1992; Birkhead et al.
1995; Pizzari et al. 2003).

The third episode of conflict over EPP arises
after fertilization and influences parental in-
vestment in offspring. Multiple paternity in a
brood potentially alters sexual conflict over pa-
rental investment because it reduces the fitness
the social male could have gained from the cur-
rent reproductive bout. However, it is debat-
able whether this translates into a reduction in
paternal care (e.g., Sheldon 2002; Griffin et al
2013), although there are clearly conflicts of
interest over the fitness consequences of EPP.
For example, theory suggests that there can be

situations under which EPP does not affect the
optimal parental investment of the male (West-
neat and Sherman 1993; Griffin et al. 2013).
On the other hand, there is some evidence
that males, on average, invest less parental care
in species with higher rates of EPP (reviewed
in Griffin et al. 2013). Finally, extrapair males
would be expected to benefit if they can cause an
increased investment by both parents beyond
their optimal levels, but it is unclear what mech-
anisms would enable them to do so facultatively.

VARIATION IN MATING PATTERNS DRIVES
EPISODES OF SEXUAL CONFLICT

In this section, we focus particularly on how
different mating patterns (including EPP) af-
fect different episodes of conflict. To do this,
we distinguish four basic mating patterns that
differ in the degree of mating fidelity and the
types of sexual conflict they generate (Fig. 3).
At one extreme is lifetime sexual monogamy—
one male and one female social partner for life,
and they mate only with each other. This mating
pattern is intriguing because, in theory, sexual
conflict should be nonexistent because the life-
time fitness interests of a paired male and female
are identical and entirely dependent once pair-
ing has occurred (Rice and Holland 1997). Se-
lection experiments with *Drosophila* support
this theory—selection lines with experimentally
imposed lifetime monogamy showed dramatic
reductions in measures of sexual conflict rela-
tive to lines with the normal polyandrous pat-
tern of mating (Holland and Rice 1999). Theory
and comparative studies also suggest that life-
time sexual monogamy is crucial for the evolu-
tion of some strong forms of altruism, such as
the helping behavior observed in social insects
and some birds (Hughes et al. 2008; Cornwallis
et al. 2010; Boomsma 2013).

Any deviations from lifetime sexual monog-
amy set the stage for sexual conflict (Holland
and Rice 1997) in two different ways (Fig. 3):
sexually monogamous matings within a re-
productive bout, but males and females change
mates between reproductive bouts, or females
mate polyandrously within a given reproductive
bout. Polyandry within a reproductive bout
Sexual Conflict from Extrapair Matings in Birds

<figure><img src="image_6.png" /><figcaption>**Figure 3.** Deviation from lifetime monogamous mating creates sexual conflict, but different mating patterns create different patterns of conflict. All deviations from lifetime monogamy potentially create sexual conflict over how much a female invests in a given reproductive bout, but polyandrous matings (including EPP) are required for conflict over both matings and fertilization.</figcaption></figure>

occurs in species both with and without pair bonds; the former is the special context referred to as extrapair matings, which gives rise to EPP. This sexual conflict framework based on mating patterns is useful because it allows us to partition the different factors that contribute to sexual conflict and identify which of them apply generally to all mating systems (except lifelong sexual monogamy) and which are unique to specific mating systems.

A couple of patterns emerge. First, sexual conflict over reproductive investment is ubiquitous in all systems in which lifetime monogamy does not occur (Fig. 3)—even without polyandrous matings, traits in males that enable them to extract levels of female parental investment above the female’s optimum can be favored, including ejaculate components that manipulate females to increase their investment in the sire’s brood (Chapman 2001; Wolfner 2002; Wedell et al. 2006), and imprinted genes that, when inherited from the male, cause an embryo to increase the extent of resource extraction from its mother (Haig and Westoby 1989; Haig 2000). Second, polyandrous matings and multiple paternity (including EPP) in a given clutch or litter generate two additional episodes of sexual conflict that are absent when females mate with only one male in a given breeding season—sexual conflict over both copulations and fertilization (Fig. 3).

That general polyandry and EPP share these distinctive episodes of conflict supports the notion that EPP is simply a special case of polyandry in matings that involve pair bonds (Schlicht and Kempenaers 2011). For the conflict over copulations, which individuals are in conflict will depend on whether EPP is female or male driven, and this will affect the types of traits that are favored. For the conflict over fertilization, the scope for flexible role-specific traits in the competing males is probably limited with regard to sperm morphology, but it could be expressed as variation in copulation rate (Briskie 1993) or ejaculate size (Parker 1990; Birkhead and Fletcher 1992).

Finally, conflict that affects male parental care is clearly influenced by EPP. This is generally true because any deviation from lifetime sexual fidelity favors traits in both sexes that lead to increased investment in a given bout by the other sex. Mechanisms to achieve this increased investment include products in male ejaculates that alter female investment (Reinhardt et al. 2009) or genomic imprinting that alters offspring physiology or behavior to extract more resources from the female (and possibly the pair male [Haig and Westoby 1989; Haig 2000]). However, when sexual conflict is driven by EPP, a reduction in parental investment by the within-pair male is favored, and
A.S. Chaine et al.

that would exacerbate the already present con-
flict over optimal parental investment by each
parent. Of course, this only applies to pair-
bonded species that show male parental care—
a situation that is widespread in birds but not
ubiquitous (Schwagmeyer et al. 1999; Cockburn
2006).

CONCLUSIONS

One of our goals in writing this review has been
to give some structure to thinking about the
kinds of traits that are expected to be favored
in response to the sexual conflict that arises
when there is extrapair mating in birds. Clearly,
many of these traits are common to conflict
when females mate multiply, whether or not
there is a social mating system that includes ex-
trapair matings. We see this as an important,
and often neglected, point both because there
is really not very much that is special about EPP
in the context of sexual conflict and because
those few traits that are special are all relevant
to conflict over parental care. This is perhaps
not so surprising because it is biparental care
that underlies the structure of socially mo-
nogamous mating systems (or polygyny with
male care), and the resolution of those conflicts
might be an important source of selection on
the evolution of fidelity in general.

Most research on the incidence of extrapair
mating—in birds, at least—has focused on try-
ing to explain why males and females might
gain a fitness advantage by seeking EPCs. In
part because promiscuity is probably the ances-
tral state (Corwallis et al. 2010), we suggest that
it might be profitable to look, instead, at fac-
tors that influence the evolution of fidelity in
birds and the reduction of sexual conflict caused
by EPP. Although within-pair sexual fidelity
might evolve for a variety of reasons (Black
1996), there would certainly be advantages
from conflict reduction in the short term that
might well outweigh the disadvantages of infi-
delity, some of which we have listed in this re-
view. Thus, we suggest that, in species with bi-
parental care in particular, models that consider
the benefits of fidelity balanced against the costs
of extrapair mating, including costs due to sex-

ual conflict, might help us to understand the
still bewildering incidence of EPP within and
among bird species.

In a similar vein, it has been clear for a long
time that demography could have a major influ-
ence on the value of extrapair mating in birds.
As Arnold and Owens (2002) showed, about
half of the variation in rates of EPP among
bird species can be explained solely by the rates
of adult mortality. Two factors might explain
this pattern. First, a prerequisite for future co-
operation between a breeding pair is that both
the male and female of a pair survive to the
following year, a probability that decreases ex-
ponentially with increased mortality rates (i.e.,
joint survival ∝ mortality²). Second, longer-
lived species simply have more opportunity to
benefit from the advantages of sexual fidelity
(i.e., more years of enjoying the benefits) and,
as a consequence, have lower rates of EPP and
EPP-driven sexual conflict—a notion that re-
mains to be explored. This, again, suggests that
an exploration of the factors that influence the
evolution of fidelity could be a profitable way
to understand the distribution of EPP both
within and among species. As we have outlined
above, traits that arise from sexual conflict vary
during the breeding cycle, involving distinct ep-
isodes of selection before copulation, between
copulation and fertilization, and during the pe-
riod of parental care. Consideration of the costs
and benefits of fidelity during each of these ep-
isodes is important because these will vary, di-
rectly influencing the benefits of sexual fidelity
during each episode.

As has been frequently pointed out, there
are many interesting parallels between the nat-
ural histories (social monogamy, biparental
care) and modes of communication (vocal and
color vision) in birds and humans (Birkhead
2012). As for birds, EPP in humans creates sex-
ual conflict that is resolved to some extent by
behaviors (mate guarding, kin recognition),
physiologies (concealed ovulation), and the ad-
vantages of sexual fidelity, particularly with re-
spect to parental care (Benshoof and Thornhill
1979; Burley 1979; Alvergne et al. 2009). We
have focused this review on sexual conflict in
birds, but we suggest that the perspectives we
have taken here—on the players, changes in conflict across episodes of the breeding cycle, and the traits that evolve to reduce conflict—are generally applicable to the study of sexual conflict in any organism in which females mate multiply.

## ACKNOWLEDGMENTS

Our research on the mating systems of birds is supported by grants from Agence Nationale de la Recherche (ANR)-LabEx "Tulip" and ANR-Programme Jeunes Chercheuses Jeunes Chercheurs (JCJC) "NetSelect" (A.S.C.), the Natural Sciences and Engineering Research Council of Canada and Queen's University (R.M.), and the National Science Foundation, National Geographic Society, and the University of California (A.S.C., B.E.L.).

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<figure><img src="image_7.png" /></figure>

# Sexual Conflict Arising from Extrapair Matings in Birds

Alexis S. Chaine, Robert Montgomerie and Bruce E. Lyon

*Cold Spring Harb Perspect Biol* published online January 20, 2015

**Subject Collection** The Genetics and Biology of Sexual Conflict

**Sexual Conflict Arising from Extrapair Matings in Birds**

Alexis S. Chaine, Robert Montgomerie and Bruce E. Lyon

**Sexual Conflict in Hermaphrodites**

Lukas Schärer, Tim Janicke and Steven A. Ramm

**Sex Chromosome Drive**

Quentin Helleu, Pierre R. Gérard and Catherine Montchamp-Moreau

**Is Sexual Conflict an "Engine of Speciation"?**

Sergey Gavrilets

**Sexual Cannibalism as a Manifestation of Sexual Conflict**

Jutta M. Schneider

**Sexual Conflict and Sperm Competition**

Dominic A. Edward, Paula Stockley and David J. Hosken

**Paradox of Mother's Curse and the Maternally Provisioned Offspring Microbiome**

Michael J. Wade

**The Relationship between Sexual Selection and Sexual Conflict**

Hanna Kokko and Michael D. Jennions

**Sexually Antagonistic Zygotic Drive: A New Form of Genetic Conflict between the Sex Chromosomes**

Urban Friberg and William R. Rice

**Sex-Biased Gene Expression and Sexual Conflict throughout Development**

Fiona C. Ingleby, Ilona Flis and Edward H. Morrow

**Sexual Conflict and Seminal Fluid Proteins: A Dynamic Landscape of Sexual Interactions**

Laura K. Sirot, Alex Wong, Tracey Chapman, et al.

**Conflict on the Sex Chromosomes: Cause, Effect, and Complexity**

Judith E. Mank, David J. Hosken and Nina Wedell

**Sexual Conflict between Parents: Offspring Desertion and Asymmetrical Parental Care**

Tamás Székely

**The Sexual Cascade and the Rise of Pre-Ejaculatory (Darwinian) Sexual Selection, Sex Roles, and Sexual Conflict**

Geoff A. Parker

**Specialists and Generalists: The Sexual Ecology of the Genome**

David Haig, Francisco Úbeda and Manus M. Patten

**Patterns and Mechanisms of Evolutionary Transitions between Genetic Sex-Determining Systems**

G. Sander van Doorn