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Research
Cite this article: Culina A, Hinde CA, Sheldon
BC. 2015 Carry-over effects of the social
environment on future divorce probability in a
wild bird population. Proc. R. Soc. B 282:
20150920.
http://dx.doi.org/10.1098/rspb.2015.0920
Received: 20 April 2015
Accepted: 16 September 2015
Subject Areas:
behaviour, evolution, ecology
Keywords:
social environment, divorce, pair formation,
great tit, mate choice
Author for correspondence:
Antica Culina
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2015.0920 or
via http://rspb.royalsocietypublishing.org.
Carry-over effects of the social
environment on future divorce probability
in a wild bird population
Antica Culina1,2, Camilla A. Hinde1,3 and Ben C. Sheldon1
1
Edward Grey Institute, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, Recanati-Kaplan Centre,
Abingdon Road, Tubney House, Tubney, Oxfordshire OX13 5QL, UK
3
Behavioural Ecology Group, Department of Animal Sciences, Wageningen University, PO Box 338,
6700 AH Wageningen, The Netherlands
2
Initial mate choice and re-mating strategies (infidelity and divorce) influence
individual fitness. Both of these should be influenced by the social environment, which determines the number and availability of potential partners.
While most studies looking at this relationship take a population-level
approach, individual-level responses to variation in the social environment
remain largely unstudied. Here, we explore carry-over effects on future
mating decisions of the social environment in which the initial mating decision
occurred. Using detailed data on the winter social networks of great tits, we
tested whether the probability of subsequent divorce, a year later, could be predicted by measures of the social environment at the time of pairing. We found
that males that had a lower proportion of female associates, and whose partner
ranked lower among these, as well as inexperienced breeders, were more likely
to divorce after breeding. We found no evidence that a female’s social environment influenced the probability of divorce. Our findings highlight the
importance of the social environment that individuals experience during
initial pair formation on later pairing outcomes, and demonstrate that such
effects can be delayed. Exploring these extended effects of the social environment can yield valuable insights into processes and selective pressures acting
upon the mating strategies that individuals adopt.
1. Introduction
The social environment has repeatedly been shown to shape individual fitness,
population dynamics and selection acting on behavioural and morphological
traits, not only in humans [1–3], but also in other animals [4–7]. One of the
main pathways for these effects is via the influence of the social environment
on reproductive success. For example, Oh & Badyaev [5] found that male
house finches (Carpodacus mexicanus) with less elaborate plumage (which are
less preferred by females) can increase their mating success if they change
winter flocks often (thus changing selection on ornamentation) [5]. Social effects
need not be immediate, but may have extended fitness consequences, even
several years after the interactions have happened. For example, the connectivity
of young long-tailed manakin (Chiroxiphia linearis) males with other males in their
social network predicted their social rise and mating success up to 8 years later [4].
The social environment should be especially important for primary mating
strategies (initial mate choice) and secondary mating strategies (divorce and infidelity) in socially monogamous species where mate sampling might be limited
and hence constrained by the social environment; such constraints might lead
to the formation of a suboptimal partnership [8].
Suboptimal partnerships in socially monogamous species can be adjusted
either by mating outside of the social pair (i.e. infidelity) and/or by divorcing
a partner after initial breeding [9–12]. Consequently, when the social environment influences initial mate choice by determining the number of opposite sex
associates [13,14], it should also influence the emergence of secondary mating
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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2. Material and methods
2
(a) Great tits
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Great tits breed in socially monogamous, territorial pairs and
spend the winter in mixed species flocks composed of variable
numbers of individuals [21]. Although the great tit is one of
the most extensively studied bird species, knowledge about the
process of pair formation, winter social behaviour and its influence on pairing outcome is still comparatively sparse. Previous
studies have indicated that breeding pairs generally form
between birds belonging to the same core winter flock [22],
mostly after the winter flocks dissolve; however, some birds
pair while still within the flock [22,23]. More recent work has
demonstrated that pairs do form throughout the winter, with
possibly several peak periods of pair formation, depending on
the winter [24]. Reported divorce rates (i.e. the rate at which
pairs that formerly bred together separate and pair with other
birds, given that both survive) in great tits vary between 0%
and 51% [25], but have been estimated at 31 – 50% in this population [26]. Divorce in great tits sometimes follows breeding
attempts with low breeding success [27,28], and happens more
often in pairs containing first year breeders (i.e. birds between
their first and second breeding season [23,29]). Two studies have
suggested that social organization in winter and winter residency
might influence divorce probability in great tits [23,25]. Both these
studies concentrated on divorce in relation to whether pair members spent winter in the same flock or not, after they had already
bred. Dhondt et al. [25] found that divorce occurred more often
in populations with lower winter residency. On the other hand,
Saitou [23] carried out more detailed observations of flocks of
colour-ringed birds. He found that divorce happened more often
in pairs that, after breeding together, belonged to different
winter flocks, but also in pairs that belonged to different flocks
before breeding.
(b) Data collection
We collected data on winter social behaviour (2007 – 2008,
2008 – 2009, 2009 – 2010, 2011– 2012 and 2012 – 2013 winters) and
breeding pairs (2008 – 2014 breeding seasons) from a free-ranging
great tit population in Wytham Woods (518460 N, 18190 W).
The breeding population of great tits at this site has been monitored since the 1960s, whereas the collection of the winter social
behaviour started, as a part of a larger project, in the 2007 winter.
As a part of this long-term project, all birds receive a standard
British Trust for Ornithology ring as well as a passive integrated
transponder (PIT-tag) when first captured, either as breeders
or nestlings during the standardized monitoring of the breeding
population [21,30,31], or during constant winter catching (mostly
immigrants). This ensured that the majority of birds wintering in
the woods were tagged (more than 80% of birds, [32]). To study
the influences of the social environment in the winter of pair
formation on the probability of a pair to divorce between breeding
seasons t and t þ 1, we needed data on winter flocks in the winter
prior to the breeding season t (e.g. data from the 2011 to 2012
winter were used to explore influences on divorce between 2012
and 2013 breeding seasons). Data on winter flocks were collected
using radiofrequency identification technology where birds
marked with PIT-tags are detected at feeders equipped with PITdetecting antennae. Tagged birds were registered at an array of
logger-equipped feeders placed at different feeding locations.
During winters 2007–2008 to 2009–2010, 16 (out of overall 67)
feeders were open (and thus available for birds) at any time
between August and March (2007–2008 winter: from 3 August
2007 to 9 March 2008; 2008–2009 winter: from 22 August 2008 to
12 March 2009; 2009–2010 winter: from 24 August 2009 to 8
March 2010). These feeders were rotated every 4 days around 67
feeding locations following a structured randomized design, so
Proc. R. Soc. B 282: 20150920
strategies. In this way, the social environment may not only
impact breeding success through the immediate effects of the
quality of the social partnership, but also through later fitness
effects of secondary mating strategies. For example, across
socially monogamous birds, divorce has been shown to lead
to an increase in reproductive success with a new partner [15].
However, the social environments of individuals, and their
subsequent effects, are challenging to study because they
require detailed knowledge of the behaviour of large numbers
of individuals. In free-ranging animal populations, data on
the social environment are difficult and time-consuming to
obtain. Consequently, studies often use a range of demographic proxies, such as sex ratio, coloniality or mortality rates
as an estimate of the social environment to which individuals
are exposed [16–18]. For example, in their recent phylogenetic
comparative analysis, Liker et al. [18] showed that divorce rates
are higher in species with a female-biased adult sex ratio [18].
While these studies have given valuable insights into the
ways demographic factors influence divorce rates at the level
of a species and populations, responses to the social environment at the individual level have received less attention.
Moreover, studies using large-scale demographic factors may
not easily quantify spatial and temporal variability in the
social environment, and do not distinguish between the demography of the environment in which a pair had formed
(i.e. before the first breeding), and of the environment in
which divorce has happened (i.e. after the first breeding).
Advances in the application of social network theory to
study heterogeneous associations within animal groups,
together with the development of new tracking technologies,
have enabled easier quantification, and statistically more
robust description, of the social environment that individuals
experience (reviewed in references [19,20]).
In this study, we used novel tracking techniques to
construct social networks in winter flocks of great tits
(Parus major) and to quantify how the social environment at
the time a pair forms predicts its future divorce probability
(i.e. after its first breeding season). The main hypotheses we
tested were as follows (i) we predicted that birds that had
had fewer associates of the opposite sex (we term this
‘between-sex degree’), or a lower proportion of the opposite
sex as associates in their winter social network prior to breeding season t, would be more likely to divorce between breeding
seasons t and t þ 1. We reasoned that a smaller number of
opposite sex associates would restrict the pool of potential partners from which to sample and choose from. Similarly, it might
be that the proportion of opposite sex associates, rather than,
or in addition to, their absolute number determines their
availability owing to competition with other males. Thus,
lower numbers, as well as a lower proportion, of opposite sex
associates should increase the incidence of suboptimal partnerships, and consequently, lead to higher divorce probability
later. (ii) We predicted that birds with a weaker association
strength with their future partner, and/or lower rank of their
future partner (in terms of the association strength) within
their opposite sex associates in the winter in which they
paired would divorce more often between breeding seasons t
and t þ 1. We reasoned that a lower association strength and,
even more importantly, lower partner association–strength
rank (the position, in terms of the association strength, a partner had on the list of all opposite sex associates) should indicate
a lower level of preference for that partner (in comparison with
other birds of the opposite sex).
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We based the description of the winter social environment on the
spatio-temporal detection of co-occurrence of individuals at feeders (i.e. gambit of the group approach [33]). We used networks
constructed using the Gaussian mixture model for event streams
(GMMEvent) method [34] to identify gathering events (representing feeding flocks) from the data collected on loggers. The
method has been shown to be a robust way to derive social
networks from spatio-temporal data streams of co-occurrences
of individuals [35]. There were 41 226 (2007– 2008), 39 046
(2008 – 2009), 12 740 (2009 – 2010), 83 152 (2011 – 2012) and
132 143 (2012–2013) such gathering events in each winter.
Gathering events were used to identify all associates of a focal individual (i.e. all other individuals seen at least once in the same
gathering event as a focal individual). For each winter, we calculated the degree (the number of individuals the focal bird
was associated with) and between-sex degree (the number of
opposite sex individuals the focal bird was associated with).
Degree and between-sex degree were strongly correlated in both
datasets and in both sexes (males: Kendall’s tau(2007 – 2010) ¼ 0.91,
p , 0.001; tau(2011 – 2013) ¼ 0.90, p , 0.001; females: tau(2007 – 2010) ¼
0.93, p , 0.001, tau(2011 – 2013) ¼ 0.92, p , 0.001). We used
between-sex degree for our analysis as it better reflects the
number of the opposite sex associates. We calculated the strength
of the association between the two individuals (i.e. between
males and females) using the half weight index (HWI) [36,37]:
HWI ¼
X
,
X þ Yab þ 1=2ðYa þ YbÞ
where x is number of gathering events where both individuals a
and b were part of the same gathering event; Ya (or Yb) number
of gathering events in which only individual a (or b) was seen,
and Yab number of times individuals were simultaneously detected
in different gathering events.
In the first three winters, we calculated the association strength
for each month, and for the 2011– 2012 and 2012–2013 winters for
each weekend of data collection. We scored partner association–
strength rank using the following procedure: first, we calculated
the association strength between the focal bird and each bird
of the opposite sex (including its future breeding partner) that
the focal bird associated with; second, we ordered these from the
highest to the lowest; third, we determined the placement (i.e.
the rank) of the focal bird’s breeding partner on the list. For
example, if the future partner association –strength rank is 1, this
means that, considering all opposite sex associations, the focal
bird associated most strongly with its future partner. We provide
the frequency distribution of partner strength, female’s and
(d) Data analysis
To test for the influence of social network traits in the winter of
pair formation (i.e. winter prior to the breeding season t) on the
probability of a pair to divorce between breeding seasons t and
t þ 1, we considered only newly formed pairs (i.e. pairs that
formed in the winter prior to the breeding season t). Calculating
association strength (and partner association– strength rank) and
determining whether a pair divorced before the next season,
required that both pair members were tagged (i.e. observable)
in the winter prior to the breeding season t, and survived (and
were seen breeding) between t and t þ 1 breeding seasons. We
excluded those pairs where one or both the pair members was
first detected in February (2007 – 2008 to 2009– 2010 winters) or
in just the last two weekends of data collection (2011– 2012 and
2012 – 2013 winters), and pairs whose members were never
seen associated (in all but two cases, these were pairs where
one member was not detected at all in winter). Consequently,
sample sizes (especially for the first three winters of data collection) were reduced despite the large number of birds tagged in
the entire population (electronic supplementary material, table
S1). Because of the small sample size, and because we were interested in the absolute number of associates of the opposite sex (i.e.
the pool of the potential breeding partners), the effect of which
should be independent of winter, we combined the first three
winters into one dataset. However, we kept the 2011 – 2012 and
2012 – 2013 winters separate from the previous three winters,
because the data-collection methods were different in these two
sets of winters. Similarly, partner association– strength rank
(that we assume relates to the level of preference of the focal
bird to associate with its partner compared with other birds of
the opposite sex), should be independent of winter too (even if
winters differ in the distribution of association strengths
among all birds). On the other hand, the association strength
between the future pair members is more likely to relate to
winter-specific effects (i.e. if the distribution of association strength
differs between different winters). Thus, we checked whether
winter had a strong influence on the association strength between
pair members (including all pairs in the network, and not only the
newly formed pairs). We compared Akaike information criterion
(AIC) values [38] of the two simple linear models with the association strength as the response, and with or without (i.e. the
intercept model) winter as the explanatory variable. We did this
for each set of winters separately (i.e. 2007– 2008 to 2009– 2010;
and 2011– 2012 and 2012–2013 winters). The two sets of models
(i.e. winter versus no winter effect on association strength)
gained similar support for 2007–2008 to 2009– 2010 winters
(AICno winter ¼ 2340.76, AICwinter ¼ 2339.66, LR test p ¼ 0.23),
further justifying the treatment of the first three winters as one
dataset. However, for the 2011– 2012 and 2012–2013 winters,
there was a winter-specific effect on the association strength
(AICno winter ¼ 2358.01, AICwinter ¼ 2363.50, LR test p ¼ 0.006).
We thus coded for three sets of winters in our analysis:
2007–2008 to 2009 –2010, 2011–2012 and 2012–2013.
We ran binomial generalized linear models, with pair status in
year t þ 1 (divorced or faithful) as a binomial response variable to
test for the variables influencing divorce probability, for each sex
separately. Because members of 62 future pairs were never
detected in the same winter flock (i.e. not associated, in all but
two cases, this was due to one of the partners not being detected
in winter), we restricted the main analysis to only those pairs
that were detected in the same flock at least once. This was necessary, as partner strength and partner association –strength rank can
3
Proc. R. Soc. B 282: 20150920
(c) Methods to describe the winter social environment
male’s partner rank, female and male between-sex degree, for winters 2007 –2008 to 2009– 2010, for the 2011–2012 winter and for the
2012–2013 winter in the electronic supplementary material,
figures S1 and S2.
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that each of eight approximately equally sized sections of the
woods always had two active loggers in it. In the 2011 –2012 and
2012–2013 winters, there were 65 feeders (same locations as previous data), all of which were simultaneously opened once a
week, for 2 subsequent days (weekends), between September
and March (in 2011 –2012 winter: from 8 September 2011 to
3 March 2012; in 2012–2013 winter: from 1 September 2012
to 3 March 2013). Over the five studied winters, feeders recorded
6 743 553 visits by 3198 tagged individual great tits. The datacollection set-up reduced the possibility that flocks would get
attracted to a constant food source, and we assume that data gathered at feeders represent a ‘snapshot’ of the social composition at
the time of feeding. Data on breeding pairs (i.e. identities of pair
members and details of their breeding parameters) were collected using standardized protocols during the breeding season
[21,30,31]. We used this information to determine the incidence
of pair fidelity (i.e. pairs that breed together in the year t and
again in the year t þ 1), and divorce (i.e. pairs that bred in the
year t, where both members survive to the next season, but
breed with different partners in the year t þ 1).
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We first compared the performance of competing models, for
each sex separately (males: electronic supplementary material,
table S2, females: electronic supplementary material, table S3)
including three main explanatory variables ( partner strength,
between-sex degree and partner association – strength rank; and
two-way interactions between partner strength and partner
rank, and partner strength and between-sex degree). We also
compared the performance of the same set of models, but with
breeding experience added as a covariate. Then, we added the
proportion of opposite sex associates (as a measure of the intensity of the competition for partners) as an interactive effect with
the between-sex degree to the main model structure, or replaced
between-sex degree with the proportion of same-sex associates
(males: electronic supplementary material table S2, females: electronic supplementary material, table S3). We controlled for the
winter block of data. We also controlled for clutch size in each
model because we have evidence [14,24] that clutch size is an
important predictor of divorce in great tits and closely related
tit species.
To additionally test for the influence of between-sex degree
and proportion of the opposite sex associates on divorce probability, we used the full dataset, including all new pairs (i.e.
irrespective of whether both partners were seen in winter or
not). Here, we also included a variable coding for whether or
not a pair was ever seen associating (list of models in electronic
supplementary material, tables S4 and S5). We ran additional
models to control for the number of weeks a bird was seen in
the network (additive or interactive effect with the between-sex
degree) and models where only birds seen in more than four
weekends were considered. These models gave results similar
to those of the main models.
We considered the model with the lowest AIC value as the
best supported one, if this value was 3 or more units lower
than the AIC of the next lowest AIC model. All statistical analysis
were done in the R package lme4 [39], and predicted values of the
response variables (with corresponding 95% CI) calculated using
the predict() function.
3. Results
The likelihood of divorce for male great tits belonging to those
pairs where pair members were seen associated in winter was
best explained by male’s breeding experience, proportion of
female associates, partner association–strength rank, partner
strength and the interaction between the last two (electronic
4. Discussion
We used a detailed dataset of associations between males
and females in winter flocks of wild great tits to describe
how the social environment, including pair bond, affects
4
Proc. R. Soc. B 282: 20150920
(i) main explanatory variables: partner HWI strength,
between-sex degree (i.e. number of opposite sex associates), proportion of opposite sex associates in the social
network of all associates, partner association –strength
rank among opposite sex associates (all of these calculated
in the winter before the breeding season t), experience of
the breeder (two possible values: bred previously, or not);
(ii) control variables: winter (three possible values: winters
2007– 2008 to 2009– 2010, 2011 – 2012 or 2012– 2013), and
clutch size (in breeding season t).
supplementary material, tables S1 and S2; estimate for the
term ¼ 213.85, z-value ¼ 22.47, p ¼ 0.013). The absolute
number of female associates (i.e. between-sex degree) did
not influence the divorce probability of a male. Divorce probability decreased with an increase in the proportion of female
associates a male had in the winter of pair formation
(figure 1a). Divorce probability also decreased as the association–strength rank of a female partner increased (figure 1b).
For example, the probability that an inexperienced male with
the lowest proportion of female associates (which was 0.38)
in the 2012–2013 winter would divorce before the next
breeding season (i.e. between 2013 and 2014) was 0.98 (95%
CI ¼ 0.39–0.99). This probability decreased to 0.22 (95% CI ¼
0.11–0.86) for a male with the highest proportion of female
associates (0.54). In the same winter, the divorce probability
ranged between 0.04 (95% CI ¼ 0.002–0.42) for an inexperienced male whose breeding partner ranked first among all
of his female associates, and 0.98 (95% CI ¼ 0.82–1) for an inexperienced male whose female ranked as 13th. A similar pattern
of increased divorce probability with a decrease in the proportion of female associates, and a decrease in partner’s
association–strength rank, was evident in experienced males,
and in other sets of winters (i.e. 2007–2009, and 2011–2012;
figure 1a,b). Finally, there was an interaction between partner
association–strength rank and partner strength. While males
whose female was ranked as their first female associate had a
low probability of divorcing (and this probability decreased
with the increase in partner strength), for males whose
female was ranked lower, the divorce probability increased
with the increase in partner strength (figure 2a,b). The divorce
probability was lower in newly formed pairs where the
male was an experienced breeder. Divorce probability of
an experienced male in a newly formed pair was 0.27 (95%
CI ¼ 0.05–0.71), and that of an inexperienced male 0.88
(0.49–0.98). To additionally test for the influence of betweensex degree and proportion of female associates on male’s
divorce probability, we considered males belonging to all
newly formed pairs (not just those that were seen associated
with their future females, as we did in the analysis above).
The results of model selection (electronic supplementary
material, table S4) gave weak support to the models where
the between-sex degree influenced males divorce probability.
In contrast to males, we found no evidence that female
social network traits, partner association–strength rank, or
her breeding experience predicted divorce probability. Neither
strength of the association with the partner, partner association–strength rank, between-sex degree, proportion of male
associates in female’s social network, nor breeding experience
of females that were observed associating with their future
breeding partners influenced divorce probability (see electronic supplementary material, table S3 for model selection).
Similarly, neither between-sex degree nor proportion of male
associates predicted divorce probability of females in new
partnerships (all females of newly formed pairs, and not just
those that were seen associated with their future breeding
partners; electronic supplementary material, table S5).
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only be estimated for those pairs that were seen associated; pairs
never seen associated in winter were not more likely to divorce
(AIC of model, controlled for clutch size and winter, was similar
in model with: AIC ¼ 139.35 and without: AIC ¼ 137.70 the variable coding for whether a pair was seen to be associated). Thus, we
assumed that these pairs represent an unbiased sample of all pairs,
where one or both pair members failed to be detected at feeders
(in 36 of these pairs one of the partners was not tagged in the
winter of interest). We considered five main explanatory variables,
and two control variables in our models:
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inexperienced male breeders
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9
–200
2007
2012
2011
2011
0.50
5
experienced male breeders
009
7–2
200
0.75
2012
0.25
0.3
0.4
0.5
0.6
0.7
0.3
0.4
proportion of female associates in male’s social network
0.5
0.6
0.7
20
2012
0.50
2011
2007–2009
2012
0.75
2011
predicted divorce probability
07
–2
00
9
(b)
0.25
1
5
10
14
partner’s rank
1
5
10
14
Figure 1. The predicted probability of a newly formed great tit pair (breeding in season t) divorcing (as opposed to staying faithful) between breeding seasons t
and t þ 1 according to (a) proportion of female associates in male’s social network, and (b) rank of male’s partner (in terms of association strength) among all of
his opposite sex associates (rank 1 is the female bird with whom the male has the strongest association), in the winter prior to breeding season t. Results are given
for inexperienced breeders (i.e. males who were recorded breeding for the first time in breeding season t) and experienced breeders, and for three sets of winters
(2007 – 2009 winters, winter 2011, winter 2012). Shaded areas on the graph represent the 95% CI of the estimate. Please note that the 95% CI of the adjacent years
overlap, leading to the darker shade of the area. The estimates were obtained from the best binomial generalized linear model, controlling for the effect of the
clutch size of a pair. (Online version in colour.)
future divorce probability. Our results showed that the male
(but not the female) social environment and the association –
strength rank of a male’s future breeding female among
his associates influenced the divorce probability of newly
formed pairs. Males with a lower proportion of female associates, and males whose future breeding partner ranked
relatively low among these, had a higher divorce probability
after the first breeding of a pair. An increase in association
strength between future breeding pair members decreased
divorce probability only if a female was the first-ranked
female associate of her male, but increased divorce probability otherwise. Previous studies on the influence of the
social environment (approximated through demographic factors) on divorce probability have not considered the social
environment in which a pair formed, but only the environment in which divorce happens. Our findings should be
considered from the three main perspectives: (i) the importance of the social environment (in terms of the possible
mating options) in mate choice; (ii) males as a sex that exercise partner preferences; and (iii) the extended influence of
the social environment in which mate choice takes place on
future reproductive decisions.
The influence of the social environment on mate choice
decisions has been studied in the context of non-independent
Proc. R. Soc. B 282: 20150920
predicted divorce probability
(a)
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5–13
(b)
k=
2
ran
3–11
rank =
0.75
6
rank =
rank
=
0.50
1
0.25
rank =
0.1
0.2
0.3
association strength
0.4
0.5
0
0.1
2
rank = 1
0.2
0.3
association strength
0.4
0.5
Figure 2. The predicted probability of divorce for a newly formed great tit pair (breeding in season t) between breeding seasons t and t þ 1 according to association strength between pair members and association – strength rank of male’s partner, among all his opposite sex associates (rank 1 is the female bird with whom
the male has the strongest association), in the winter prior to breeding season t for (a) inexperienced males; (b) experienced males. The probability is plotted for all
years (2007 – 2013) combined. The estimates were obtained by the best binomial glm, controlling for the effect of the clutch size and winter (winters 2007– 2009,
winter 2011 and winter 2012).
mate choice (commonly mate choice copying, [40]), and the
relative attractiveness of a male compared with his associates [5,8,41]. Both empirical and theoretical work on these
two aspects has emphasized that social influences on mate
choice can substantially affect sexual selection [8,40].
A third aspect of the social influence on mate choice is the
number (and quality) of possible partners [42]. For example,
the frequency of extra-pair fertilizations in a house finch
population was found to be largely determined by the availability of suitable extra-pair mates [43], and is thus specific
for each individual in the population. Our study demonstrates that divorce, which can be considered as a form of
mate choice [10], and a way to correct for a suboptimal
mating situation [15], may also depend on aspects of the
social environment in which initial mate choice happens.
Our finding that males with a lower proportion of female
associates during the period of pair formation divorced
more often after breeding indicates that the intensity of
competition (which we expressed as the proportion of the
opposite sex associates) may limit the possibilities available
for preferred pairing, regardless of the absolute number of
female associates. However, there are other explanations,
such as the possibility of a correlation between personality,
social behaviour [44] and divorce probability. More detailed analysis of the composition of flocks and the way the
composition changes over winter could help to reveal the
mechanism behind our findings. Finally, when we looked
at males of all new pairs, which also included those males
for which we did not have information on the association
strength with their females (mainly because she was not
recorded in the network), the effect was no longer significant.
One possible explanation is that the effect of the proportion
of the opposite sex associates can be detected only when
the data on the association between pair members are fully
known. The support for this claim also comes from the results
of the main model selection; if the information on partner
strength and association –strength rank were excluded,
the proportion of female associates was not selected as a covariate influencing divorce probability. However, why this
might be so is not fully clear. A likely explanation is that
the effect of the proportion of female associates explains the
significant amount of the variance that remains after the
effect of partner strength and association –strength rank are
accounted for.
Although mate preferences have traditionally been
studied in females [40,45], there is increasing evidence that
males might be choosy [46], especially in social monogamous
species where both parents care for offspring [47]. Results of
some studies indicate that divorce, as a type of secondary
mate choice, could also to be driven by both sexes [48]. For
example, while divorce seems to be female driven in blackcapped chickadees (Poecile atricapillus), where females abandon their partner for a male of higher quality [49], it is
thought to be driven by males in house wrens, Troglodytes
aedon [50]. Our result, that the male’s but not the female’s
level of preference for the future breeding partner (as inferred
from association –strength rank) influenced the probability
of divorce after their first breeding, indicates that males
likely use divorce to correct for suboptimal partnerships.
Low partner association –strength rank of a female among
other female associates most likely reflects the situation
where a male was not able (because of competition or/and
female choice) to breed with his preferred female, and
ended up breeding with a less preferred one. Interestingly,
while low partner association–strength rank was related to
the high divorce probability in all three sets of winters,
males that had their partners ranked high were more likely
to divorce in the first 3 years (i.e. 2007–2009) than in the
later years of data collection. This difference in the magnitude
of the effect of partner association –strength rank on the divorce probability could likely be connected to the difference in
the time periods when most future pairs start associating, and
thus expressing partner preferences (see reference [23]).
Exploring finer temporal changes in partner association –
strength rank, and keeping track of the most preferred
female over time would be a good way to study the observed
pattern in more detail.
The lack of any influence of the components of the social
environment on female divorce probability is difficult to
explain, but we suggest several possible reasons for this.
First, in great tits, males hold territories, and because of
this, females that divorce their males, in general, also change
Proc. R. Soc. B 282: 20150920
0
rspb.royalsocietypublishing.org
predicted divorce probability
(a)
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5. Conclusion
7
Data accessibility. Data are available on Dryad, doi:10.5061/dryad.1s5rh.
Authors’ contributions. A.C. participated in data collection, performed the
main data analysis and wrote the main manuscript. C.A.H. and
B.C.S. participated in data collection, and interpretation of the data.
All three authors contributed substantially to revisions.
Competing interests. We declare we have no competing interests.
Funding. This work was funded by an ERC Advanced grant no. (AdG
250164) to B.C.S.
Acknowledgements. We thank Reinder Radersma for the advice on the
data analysis. We thank Joshua Firth and Damien Farine for constructing the social networks and generating the association matrix
that formed the basis of our subsequent analyses. We are grateful
to all the people that helped to collect data on social winter behaviour
and breeding data of great tits in Wytham woods.
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