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\begin{document}

\title{Divorce is linked with extra-pair paternity in a monogamous passerine}



\author[1]{Jamie Dunning}%
\author[2]{Terry Burke}%
\author[1]{Julia Schroeder}%
\affil[1]{Imperial College London}%
\affil[2]{The University of Sheffield}%


\vspace{-1em}



  
  \date{June 18, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
The question of why socially monogamous females engage in extra-pair
behaviour is long-standing in evolutionary biology. Recent theoretical
work has moved away from the indirect-benefits hypothesis to explain
female extra-pair behaviours, instead favouring suggestions that they
are the result of pleiotropic effects. That is, a trait under strong
positive selection in either or both sexes are genetically linked to
another, often unrelated, trait. For example, where genes beneficial to
female fecundity (contributing to within-pair solicitation of her social
partner) are linked with extra-pair behaviour (soliciting copulations
from extra-pair males). Here, we test two predictions from this
hypothesis: We test the prediction that female divorce, measured from
the number of social mates within a given year, is linked with (1) the
number of extra-pair males and (2) the proportion of her offspring that
are extra-pair. Our results suggest that females who frequently divorce
social partners are more likely to produce extra-pair offspring than
those who maintain social monogamy. However, by contrast, those females
do not also have a higher proportion of extra-pair offspring. The number
of broods initiated was also positively correlated with extra-pair
males, probably through increased opportunity for extra-pair males to
sire offspring over a longer breeding season. Our results provide an
empirical example of a behavioural trait, beneficial to female
fecundity, that is linked with extra-pair behaviour. These empirical
results support the intrasexual pleiotropy hypothesis as a driver of
female extra-pair behaviour.%
\end{abstract}%



\sloppy


Title: Divorce is linked with extra-pair paternity in a monogamous
passerine

Abstract

The question of why socially monogamous females engage in extra-pair
behaviour is long-standing in evolutionary biology. Recent theoretical
work has moved away from the indirect-benefits hypothesis to explain
female extra-pair behaviours, instead favouring suggestions that they
are the result of pleiotropic effects. That is, a trait under strong
positive selection in either or both sexes is genetically linked to
another, often unrelated, trait. For example, where genes beneficial to
female fecundity (contributing to within-pair solicitation of her social
partner) are linked with extra-pair behaviour (soliciting copulations
from extra-pair males).

Here, we test two predictions from this hypothesis: We test the
prediction that female divorce, measured from the number of social mates
within a given year, is linked with (1) the number of extra-pair males
and (2) the proportion of her offspring that are extra-pair. Our results
suggest that females who frequently divorce social partners are more
likely to produce extra-pair offspring than those who maintain social
monogamy. However, by contrast, those females do not also have a higher
proportion of extra-pair offspring. The number of broods initiated was
also positively correlated with extra-pair males, probably through
increased opportunity for extra-pair males to sire offspring over a
longer breeding season. Our results provide an empirical example of a
behavioural trait, beneficial to female fecundity, that is also linked
with extra-pair behaviour. These empirical results support the
intrasexual pleiotropy hypothesis as a driver of female extra-pair
behaviour.

Background

{\label{background}}

Since extra-pair paternity was first demonstrated using genetic
finger-printing to allocate parentage to a house sparrow \emph{Passer
domesticus} (hereafter sparrow, Burke, and Bruford 1987)\emph{,} the
question of why females in socially monogamous breeding systems engage
in promiscuous behaviour still presents a challenge to evolutionary
biologists (Griffith, Owens and Thuman 2022; Brouwer and Griffith 2019).
Sexual selection dictates that females should choose a reproductive
partner to maximize the fitness benefits he provides either directly to
them, through parental care, or through a high-quality breeding
territory (M\selectlanguage{ngerman}øller 2000; Nakagawa et al. 2007; Brouwer and Griffith
2019). Other benefits can be incurred indirectly, by providing offspring
with high-quality genes from the male. However extra-pair males, those
from outside an established pair bond, can only provide indirect
benefits to females. That is, extra-pair males may sire offspring
without investing in costly parental care (Lebigre, Arcese, and Reid
2013; Raj Pant et al. 2022; Table 1), the good genes hypothesis predicts
that they should signal a better (Hamilton and Zuk 1982; Birkhead 1995;
Kirkpatrick and Barton 1997), or more compatible (Blomqvist et al. 2002;
Ihle, Kempenaers, and Forstmeier 2015; but also see Griffith and Immler
2009) proposition than her social partner.

However, these predictions -- that offspring produced by extra-pair
matings, and extra-pair males themselves, are of superior quality than
within-pair offspring, and within-pair males, respectively -- are not
well supported by empirical evidence (Hsu et al. 2015; Grinkov et al.
2022). This is highlighted by multiple meta-analyses on the topic,
(Akçay and Roughgarden 2007; Arct, Drobniak, and Cicho\selectlanguage{polish}ń \selectlanguage{english}2015), and
subsequent discussion in the field (Drobniak, Arct, and Cicho\selectlanguage{polish}ń \selectlanguage{english}2015;
Griffith 2015; Nakagawa, Schroeder, and Burke 2015; Reid 2015; Brouwer
and Griffith 2019). Further, several empirical studies have suggested
costs rather than indirect benefits, to extra-pair offspring (Schmoll et
al. 2009; Sardell et al. 2012; Hsu et al. 2014), and to promiscuous
females (Forstmeier 2007; Matysiokov\selectlanguage{ngerman}á and Reme\selectlanguage{polish}š \selectlanguage{english}2013; Schroeder et al.
2016). Yet, females actively seek extra-pair copulations (Lifjeld and
Robertson 1992; Forstmeier 2007, Girndt et al. 2018), and to date, the
mechanism that drives these behaviours in females remains unresolved.

Several alternative hypotheses have sought to explain why female
extra-pair behaviours persist. For example, insurance against the death-
(Petrie and Kempenaers 1998) or infertility (Wetton and Parkin 1991;
Sheldon 1994; Vedder 2022; Table 1) of a social partner may motivate
females to seek extra-pair copulations, maintained through indirect
selection (Kempenaers and Schlicht 2010). The social environment may be
another mediator of extra-pair behaviour (Maldonado-Chaparro et al.
2018; Table 1), where individuals with high sociality - their propensity
to associate with others -- likely have more opportunity to choose
partners from larger pools of potential mates. Accordingly, the number
(Oh and Badyaev 2010; Dunning et al. 2023) and quality (Firth and
Sheldon 2016; Beck, Farine, and Kempenaers 2021) of social associations
were empirically shown to be linked to reproductive success, including
extra-pair mate choice (Beck, Farine, and Kempenaers 2020). Empirical
studies generally find that extra-pair partners are more likely to be
close neighbours (Westneat and Sherman 1997; Schlicht, Valcu, and
Kempenaers 2015; Mingju et al. 2017; Beck, Farine, and Kempenaers 2020;
Beck, Valcu, and Kempenaers 2020), adding weight to the role of
opportunism in extra-pair copulation (as empirically demonstrated by
Foss\selectlanguage{ngerman}øy, Johnsen, and Lifjeld 2006; and theoretically by Brommer et al.
2007; 2010).

Alternatively, the benefits of female extra-pair behaviour may be
explained by non-adaptive hypotheses, for example through antagonistic
pleiotropy (Halliday and Arnold 1987; Arnqvist and Kirkpatrick 2005),
where extra-pair behaviours are controlled by linked sets of genes and
selected for in one or both sexes. The intersexual (between-sex)
antagonistic pleiotropy hypothesis (Halliday and Arnold 1987; Reid and
Wolak 2018; Table 1) posits that female extra-pair behaviours are
controlled by sets of genes present in both sexes and selected where the
benefit to one sex outweighs the cost to the other (Halliday and Arnold
1987; Reid and Wolak 2018; Wang et al. 2020). For example, where the
benefit of extra-pair copulations for males, outweighs the cost of the
behaviour in females who inherit the genes from their fathers.
Intersexual antagonistic pleiotropy is a common driver of behavioural
traits (Poissant, Wilson, and Coltman 2010). Early empirical studies
into non-adaptive explanations for female extra-pair behaviour suggested
a role for intersexual pleiotropy (Forstmeier et al. 2011), but
subsequent work from the same system later suggested that intrasexual
(or within-sex) pleiotropic effects may better explain female extra-pair
behaviour (Wang et al. 2020).

Similarly, the intrasexual antagonistic pleiotropy hypothesis posits
that a trait under selection is genetically linked to another trait in
the same sex, where the benefits of one trait outweigh the cost of the
other trait (Halliday and Arnold 1987; Forstmeier et al. 2014; Wang et
al. 2020; Table 1). In this case, female extra-pair behaviour could be
pleiotropically linked with female fecundity. This would be the case,
for example, where female responsiveness to male courtship is
pleiotropically linked with increased solicitation of copulations,
enhancing fertilization success also in a within-pair context, and
extra-pair behaviour may persist (suggested by Wang et al. 2020; Bolund,
Schielzeth, and Forstmeier 2012)

Although quantitative genetic evidence for the antagonistic pleiotropy
hypotheses is described from captive experiments (Forstmeier et al.
2011; Wang et al. 2020), evidence from wild systems is scarce. Reid et
al. (2018) found no relationship between genes beneficial to male
reproductive success and female extra-pair behaviour (an example of
intersexual antagonistic pleiotropy). Further, quantitative approaches
to understanding pleiotropic effects on female extra-pair behaviours
have resulted in inconclusive effect sizes, for two reasons: First, the
heritability of male and female promiscuity is closely related to
fitness, masking any evidence of pleiotropy effect (Reid et al. 2011;
Reid 2015; Dobson et al. 2023); And second, studies with genetic
pedigrees from wild populations are scarce and have few generations,
resulting in inconclusive effect sizes (Reid et al. 2011; Moiron,
Charmantier, and Bouwhuis 2022; Dobson et al. 2023), even where
prevalence of extra-pair behaviour is high. However, if pleiotropic
effects are driving female extra-pair behaviour, then the expression of
two linked behaviours should be empirical -- if not genetically --
detectable in wild systems.

Because extra-pair behaviours are common in passerine birds (Griffith,
Owens, and Thuman 2002; Cockburn 2006; Smith 1988; Forstmeier 2007),
they are an excellent model system for testing hypotheses relating to
sexual selection and extra-pair behaviour. Here, we used a wild house
sparrow population with a twenty-year genetic pedigree to test the
prediction that extra-pair behaviours are correlated with social mate
choice (suggested by Wang et al. 2020), an assumption of the intrasexual
antagonistic pleiotropy hypothesis. Sparrows have high rates of
extra-pair paternity (Hsu et al. 2014; Hsu et al. 2015; Girndt 2018) and
are considered a model organism for studies on behaviour, life history,
and sexual selection (Sánchez-Tójar, Schroeder, and Farine 2018; Hanson
et al. 2020). In this study, we test that female propensity to switch
social partners within a breeding year (hereafter, divorce), a trait
with a potential genetic basis (Germain, Wolak, and Reid 2018) and a
proxy for mate choice, is linked with extra-pair behaviour. First, we
tested that divorce is linked with the number of extra-pair offspring,
then with extra-pair males. We carried out our study in a closed house
sparrow system, with a near-complete genetic pedigree spanning 20 years.

Table 1. Hypotheses referenced in this manuscript, see Brouwer and
Griffith (2019) for a comprehensive review.\selectlanguage{english}
\begin{longtable}[]{@{}lll@{}}
\toprule
Referenced Hypotheses & Description & References\tabularnewline
\midrule
\endhead
Good genes & Extra-pair partners that signal a greater genetic
proposition than the social male is sought to provide indirect benefits
to her offspring & (Hamilton and Zuk 1982; Birkhead 1995)\tabularnewline
Fertility insurance & Extra-pair copulations are sought to protect
against infertility in her own social partner, with or without phenotype
cues & (Wetton and Parkin 1991; Sheldon 1994; Vedder
2022)\tabularnewline
Sociality as a mediator of variation in extra-pair behaviour & The
social environment provides a mechanism for extra-pair behaviour through
increased mate-choice. & (Maldonado-Chaparro et al. 2018)\tabularnewline
Intersexual antagonistic pleiotropy & Non adaptive female extra-pair
mating derived of alleles where the cost of extra-pair behaviour to
females is small relative to the benefit to males. & (Halliday and
Arnold 1987; Forstmeier et al. 2014; Wang et al. 2020)\tabularnewline
Intrasexual antagonistic pleiotropy & Female extra-pair behaviour is
derived of alleles traits beneficial to female fecundity, for example
solicitation of social partners (considered here). & (Forstmeier et al.
2014; Wang et al. 2020)\tabularnewline
\bottomrule
\end{longtable}

\par\null

Methods

System

{\label{system}}

We systematically monitored a population of house sparrows \emph{Passer
domesticus} on Lundy Island in the Bristol Channel, UK (51.11N, 4.40W),
since 2000 (see Nakagawa et al. 2007; Ockendon, Griffith, and Burke
2009; Schroeder et al. 2012; Dunning et al. 2023). The sparrows on Lundy
breed in nesting boxes, arranged into neighbourhoods broadly defined by
building infrastructure or linear features. Females are socially
monogamous, but genetically promiscuous (Schroeder et al. 2016), and, on
Lundy, most have 2-3 broods of 4-5 eggs per breeding season (Westneat et
al. 2014).

We collected tissue samples from nestlings at the natal site and from
recaptured birds post-fledging and used the DNA extracted from those to
allocate paternity with the help of \textgreater{}22 microsatellite loci
(Dawson et al. 2012). We then constructed a near-complete genetic
pedigree (see Schroeder et al. 2015), spanning 19 years, 2000 - 2019.
All sparrows are fitted with a unique sequence of three coloured leg
rings and a British Trust for Ornithology (BTO) coded metal ring (for
details see Simons et al. 2015), which allowed us to later identify
social pairs at the nest box. Dispersal to and from Lundy Island is
limited. This, and our systematic and thorough monitoring, allowed us to
determine the exact age of birds in years, and to know when they died,
either from the rings of birds found dead or, defined as when ringed
birds were not observed for more than two years (see Simmons et al
2015).

To measure female divorce, we first excluded females that only had a
single brood, and thus, no opportunity to divorce their social mate. We
also excluded 17 females that divorced mates following the death of
their social partner, where the death of a social male occurred during
the female breeding year. We removed offspring whose parents (either
social or genetic) were missing or uncertain. We defined a divorce event
where a female paired socially with a new male to that of her previous
social partner, between broods but within years. This resulted in 353
female breeding years. These female years represented 920 broods by 190
females, 205 social fathers and 309 genetic sires between 2004 and 2019.

We defined a chick as extra-pair where they survived to the point of
sampling on day two and the confirmed social- differed from the genetic
father (the sire) in our pedigree. We counted the number of extra-pair
offspring and the number of both social and extra-pair fathers within
females within years (female years).

\par\null{\label{section}}

Models and permutations

{\label{models-and-permutations}}

To empirically test if females that divorce more often were also more
likely to produce extra-pair offspring, as implied by intrasexual
antagonistic pleiotropy theory, we ran two GLMM models with Bayesian
Markov Monte-Carlo simulations, using MCMCglmm in R (Hadfield 2010; R
Core team 2023):

\textbf{The association of divorce with extra-pair paternity} - To
examine the link between female year divorce and extra-pair paternity,
and because MCMCglmm cannot easily deal with proportion data, we ran a
multinomial model with the number of extra-pair and social offspring per
female year as response variables (see Hadfield 2010). We fitted female
divorce, measured as the number of social partners within a female year,
the number of broods she initiated, to control for increased opportunity
for extra-pair offspring, and her age in years since hatching, to
compensate for the effect of age on reproductive value (Hsu et al.
2017), as fixed effects. We also included Female ID and breeding year as
random effects on the intercept to account for variation within those
groups.

\textbf{The effect of divorce on extra-pair male engagement} - To
examine the link between female divorce and engagement of extra-pair
partners, we used a bivariate model structure, with the number of
extra-pair partners within a given female year as the response variable.
We again fitted female divorce, the number of broods initiated and her
age in years since hatching as fixed effects. Female ID and breeding
year were again modelled as random intercepts to account for variation
within those groups. We first ran models using a Poisson distribution
and logit link function, but those models failed to converge. Instead,
we used a Gaussian distribution and link function and output estimates
between the Poisson and Gaussian models were equivalent.

For all models, we used the default priors of the MCMCglmm package, and
ran over 343,000 iterations, with a burn-in of 34,000 and a thinning
interval of 200. We checked the posterior trace plots to ensure that
autocorrelation was below 0.1 and that the effective sample sizes ranged
between 1,000 and 2,000. The fixed effects were considered statistically
significant when the 95\% credible interval (CI) of its posterior
distribution did not span zero.

To test that our results were biologically meaningful, and not the
outcome of random chance, we ran a series of permutations. We removed
the link between female ID and reproductive traits by building random
matrices between males and females to re-run our models. First, we
simulated 1000 breeding events, by shuffling the number of offspring and
extra-pair offspring between females while maintaining age structure. We
then repeated these steps to simulate the number of extra-pair partners
for each female. For each permutation, we ran an identical GLMM model to
those described above. We dropped the bottom 2.5\% of the lower credible
intervals, and the top 2.5\% of the upper credible intervals, to leave
95\% of the 1000 credible intervals. We then extracted the minimum lower
and maximum upper credible interval and the mean estimate. We
interpreted significance -- that is, our results were unlikely to have
occurred by chance -- where the observed posterior mean fell outside the
span of the permuted credible intervals.

\par\null

Results

From 533 female breeding years, we identified 4963 offspring of known
social and genetic parentage including 932 extra-pair offspring, 1.7 per
female year (0 -- 11, sd: 1.77), from 1403 broods (2.6 per female year,
sd: 0.68). Females who engaged in extra-pair behaviour had a mean of 2.5
extra-pair offspring per female year (1 -- 11, sd: 1.6). Within female
breeding years, 120 females divorced their social partners on at least
one occasion (110 once, and 10 twice, 1.24 per social partners female
year: sd 0.47), where 413 remained faithful to a single social partner
over multiple broods within a female year.

Neither the number of social fathers nor the number of broods was
significantly linked with the proportion of extra-pair offspring that
hatched within a female year. However, the number of social fathers and
the number of broods per female year were positively linked to the
number of extra-pair partners she chose within a breeding year. The log
odds of having an extra-pair partner increased by 0.43, or 1.54
extra-pair partners, per social partner, and by 0.24, or 1.27 extra-pair
partners per brood respectively (Figure 1). Female age was not linked to
either the proportion of extra-pair offspring or the number of
extra-pair sires.

Neither the number of broods nor the number of social fathers was
associated with the number of extra-pair partners in our randomizations.
The observed estimates all fell outside of the simulated confidence
intervals (Figure 1). Observed posterior means fell outside of simulated
95\% confidence intervals for both broods (0.27, -1.29 -- 0.13) and
social fathers(0.81, -0.00 -- 1.86), implying that our results are not
the result of chance. Our results support the hypothesis that females
who divorce social partners regularly also engage more extra-pair males
than those who maintain social monogamy.

\textbf{Hosted file}

\verb`image1.emf`  available at \url{https://authorea.com/users/622021/articles/645321-divorce-is-linked-with-extra-pair-paternity-in-a-monogamous-passerine}

Figure 1. We interpreted significance in GLMM model outputs where 95\%
credible intervals did not span zero (red bars; otherwise black bars
denote non-significant results), and points denote posterior mean. Our
observed results (A1-2) suggest that female birds who divorce social
partners regularly engage with more extra-pair males than those who
maintain social monogamy. Likewise, the number of broods initiated also
significantly predicted an increase in extra-pair males, without
affecting the proportion of extra-pair offspring, presumably by virtue
of opportunity (A2; red bars). Simulated breeding events (B1-2), where
extra-pair males and extra-pair offspring were permuted between females
in our system were not significant. Random effects are given in the
shaded box (Dam and Cohort) for each model. Intercept and residuals for
each model are not shown in the figure: A1, intercept -1.65 (-2.12 --
-1.1), residuals 0.61 (-2.11 -- 0.92); A2, intercept -1.65 (-2.11 --
-1.8), residuals 0.53 (3.47 -- 0.72); B1, intercept -0.5 (-8.78 --
-0.14), residuals 0.81 (6.54 -- 0.95); B2, intercept 1.26 (8.53 --
1.66), residuals 1.06 (9.37 -- 1.2).

Discussion

{\label{discussion}}

We empirically tested an assumption of the intrasexual antagonistic
pleiotropy hypothesis - that extra-pair behaviour is linked to another
trait beneficial to female fecundity, in this case, solicitation of
social partners~(Halliday and Arnold 1987; Wang et al. 2020), which we
measured as the rate of divorce within years. Our results suggested that
female divorce is linked with females engaging more extra-pair males.
However, we found no effect of divorce on the proportion of extra-pair
offspring. We also found a link between the number of broods initiated
and female engagement of extra-pair males, which we consider a
by-product of the opportunity for more extra-pair paternity over a
longer breeding period.

Opportunity has been demonstrated to increase extra-pair behaviour in
several systems~(see Maldonado-Chaparro et al. 2018), including
empirical studies suggesting that extra-pair copulations may be
obligate, where they are facilitated by opportunity~(Foss\selectlanguage{ngerman}øy, Johnsen,
and Lifjeld 2006). Liker, Freckleton, and Székely (2014) suggested that
the sex ratio of the wider social environment also influences the
divorce rate, driven by female-biased sex ratios and infidelity, by
male-biased sex ratios (but also Culina, Hinde, and Sheldon 2015).
However, opportunity cannot explain what drives extra-pair
decision-making, instead, that must come from selective advantage to
those who engage in extra-pair copulations. Our results support the
suggestion by Wang et al.~(2020) that female social solicitation
behaviours are linked with extra-pair mate solicitation, and therefore,
support intrasexual antagonistic pleiotropy as a mechanism for female
extra-pair behaviour. However, we suggest that other, probably
post-copulatory, processes control the proportion of extra-pair
offspring born to females within a breeding year. Equivalent attention
has also been given towards intersexual pleiotropic effects, where
female extra-pair behaviour may be linked with a trait which benefits
male reproductive success, these studies have found little support in
captivity~(Wang et al. 2020), or in wild populations~(Zietsch et al.
2015; Reid and Wolak 2018). Where quantitative genetic studies have
sought to demonstrate a heritable basis for male extra-pair behaviour,
required for intersexual pleiotropy to drive female extra-pair
behaviour, estimates are low~(Reid et al. 2011; Reid and Wolak 2018;
Grinkov et al. 2020). However, Dobson et al..~(2023) found that the
inclusion of social partner indirect genetic effects (those derived from
the behaviour of another) improved model fit for the heritability of
both male and female extra-pair behaviour, implying a role for the wider
social environment in the plasticity of extra-pair behaviour.

We used divorce rate within a female breeding year, between multiple
broods, as a measure of solicitation, but not between breeding years -
more akin to a classic definition of divorce behaviour. Divorce is more
broadly defined as where both partners are alive, and at least one of
them has paired with a new social partner~(Black and Hulme 1996; but
also see Culina, Radersma, and Sheldon 2015). However, the motivations
for female sparrows to divorce social partners between broods may be
like those described elsewhere for divorce, which has been demonstrated
to represent an adaptive strategy between sexes across monogamous
birds~(Choudhury 1995; Culina, Radersma, and Sheldon 2015; Mercier,
Yoccoz, and Descamps 2021; Wilson, Nguyen, and Burley 2022). Previous
works have also considered divorce and extra-pair behaviours as linked
traits in the context of indirect benefits~(Cezilly and Nager 1995;
Choudhury 1995), that is, both provide females with a mechanism to
improve the quality of their social partner, by divorcing or cuckolding,
lesser quality males. However, empirical evidence for indirect benefits
derived from extra-pair behaviours is scarce~(Akçay and Roughgarden
2007; Arct, Drobniak, and Cicho\selectlanguage{polish}ń \selectlanguage{english}2015), and multi-paternity broods were
not linked to the divorce rate~Ramsay et al. (2000).

Although we consider our data to be near-complete, our phenotypic study
is still subject to some bias (Hadfield 2008). For example, we sampled
chicks for paternity at day two, (see Dunning et al. 2023), but this may
still exclude an invisible fraction of those pairs, females~(Kidd et al.
2015)~or eggs~(Yuta et al. 2018; Assersohn et al. 2021)~who fail early.
As a result, our study measures extra-pair paternity, and not extra-pair
copulations, which could be more frequent than is reflected in paternity
analysis~(Foss\selectlanguage{ngerman}øy, Johnsen, and Lifjeld 2006; Girndt 2018). Females that
exhibit extra-pair behaviours may not always produce extra-pair
offspring, but their within-pair offspring will inherit her genes, which
may determine the extra-pair behaviour. Future work may support
intrasexual pleiotropy as a mechanism for female extra-pair behaviour by
either including measures of copulation attempts (rather than paternity)
or, through further quantitative genetic methods.

We demonstrate that females who swap mates more frequently within
breeding years engage more extra-pair males, but do not have greater
proportions of extra-pair offspring. Our study contributes an empirical
example to the growing body of research that supports non-adaptive
phenomena as mechanisms for why females engage in extra-pair behaviours.

\par\null{\label{section-1}}

Bibliography

{\label{bibliography}}

Akçay, Erol, and Joan Roughgarden. 2007. ``Extra-Pair Paternity in
Birds: Review of the Genetic Benefits.'' \emph{Evolutionary Ecology
Research} 9 (5): 855.

Arct, Aneta, Szymon M Drobniak, and Mariusz Cicho\selectlanguage{polish}ń. \selectlanguage{english}2015. ``Genetic
Similarity Between Mates Predicts Extrapair Paternity---a Meta-Analysis
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