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
Since extra-pair paternity was first demonstrated using genetic
finger-printing to allocate parentage to a house sparrow Passer
domesticus (hereafter sparrow, Burke, and Bruford 1987), 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 (Møller 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 Cichoń 2015), and
subsequent discussion in the field (Drobniak, Arct, and Cichoń 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; Matysioková and Remeš 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
Fossøy, 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.