JOURNAL OF

AVIAN BIOLOGY
Communication
Extra-pair offspring are less heterozygous than within-pair
offspring in American redstarts Setophaga ruticilla
Adrianne Hajdasz, Ann E. McKellar, Laurene M. Ratcliffe, Peter T. Boag, Peter P. Marra
and Matthew W. Reudink

A. Hajdasz and M. W. Reudink (https://orcid.org/0000-0001-8956-5849)  (mreudink@tru.ca), Dept of Biological Sciences, Thompson Rivers Univ.,
Kamloops, Canada. – A. E. McKellar, Canadian Wildlife Service, Environment and Climate Change Canada, Saskatoon, Canada. – L. M. Ratcliffe
and P. T. Boag, Dept of Biology, Queen’s Univ., Kingston, Canada. – P. P. Marra, Migratory Bird Center, Smithsonian Conservation Biology Inst.,
Washington, USA.

Journal of Avian Biology
2019: e02084
doi: 10.1111/jav.02084

Subject Editor: Alexandre Roulin
Editor-in-Chief: Jan-Åke Nilsson
Accepted 14 March 2019

The vast majority of bird species are socially monogamous; however, extra-pair paternity is nearly ubiquitous and a number of theories have been proposed to explain
the prevalence of this mixed mating strategy. Here, we test the genetic compatibility
hypothesis – the idea that females seek extra-pair copulations with males whose genes
are more compatible with her own. For this study, we examined eight years of paternity data (2004–2011) from a Nearctic-Neotropical migratory bird, the American
redstart Setophaga ruticilla, breeding in southeastern Ontario, Canada. We predicted
that females paired with genetically similar males (higher relatedness) would be more
likely to produce extra-pair offspring and that extra-pair offspring would have higher
levels of heterozygosity than within-pair offspring. Alternatively, because this population experiences high levels of immigration, females may produce extra-pair offspring
with more genetically similar males because of the potential for outbreeding depression. Using five highly variable microsatellite markers, we examined patterns of relatedness among social pairs as well as measures of offspring heterozygosity. In contrast
to our predictions, we found no difference in relatedness between social pairs where
the females produced extra-pair offspring and social pairs where the females produced
only within-pair offspring. However, extra-pair offspring were significantly less heterozygous than within-pair offspring. Together, these findings suggest that females a) are
not engaging in extra-pair fertilizations based on relatedness to their social mate and
b) appear to be mating with extra-pair males that are more genetically similar to themselves. We suggest there may be benefits for females to mate with genetically similar
extra-pair males in highly outbred populations with high rates of immigration, such
as for maintaining co-adapted gene complexes or genes coding for local adaptations.
Keywords: American redstart, extra-pair paternity, heterozygosity, microsatellite,
Setophaga ruticilla

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www.avianbiology.org

© 2019 The Authors. Journal of Avian Biology © 2019 Nordic Society Oikos

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Introduction
In many bird species, females form monogamous social
bonds with their mates; however, in over 75% of these
species, females mate with extra-pair males as part of a
mixed-mating strategy (Griffith et al. 2002). Because of
the frequency and ubiquity of extra-pair mating, many
hypotheses have been developed to explain why females may
engage in extra-pair paternity, including fertility insurance
(Krokene et al. 1998), healthy mates (Reynolds and Gross
1990), good genes (Hamilton 1990, Zeh and Zeh 2001),
sexy sons (Weatherhead and Robertson 1979), and genetic
compatibility (Kempenaers et al. 1999). According to the
genetic compatibility hypothesis, females may seek extrapair copulations with males whose genes are more compatible with her own. One way mate incompatibility can arise is
through inbreeding, which can lead to the loss of heterozygosity (genetic diversity) and the accumulation of deleterious
homozygous recessive alleles (Charlesworth and Charlesworth
1987). Even in populations that are not inbred, maintaining heterozygosity has been positively linked to various fitness-related traits (reviewed in Reed and Frankham 2003).
Therefore, it may be beneficial for females to mate with
extra-pair males that are more genetically dissimilar to themselves to increase the heterozygosity of their offspring. For
example, splendid fairy wren Malurus splendens females who
were more genetically similar to their social mates were more
likely to have extra-pair offspring (EPO), and these offspring
were more heterozygous than within-pair offspring (WPO)
(Tarvin et al. 2005). Similarly, in blue tits Cyanistes caeruleus
extra-pair offspring were more heterozygous than within-pair
offspring, and also had higher fitness (Foerster et al. 2003).
Alternatively, in open, outbred populations it may be
more beneficial to females to mate with more genetically
similar males, preserving locally-adapted genes or co-adapted
gene complexes (Price and Waser 1979, Frankham 1995).
Several studies in open, potentially outbred populations such
as in tree swallows Tachycineta bicolor (Barber et al. 2005),
pied flycatchers Ficedula hypoleuca (Rätti et al. 1995), and
waved albatross Phoebastria irrorata (Huyvaert and Parker
2010) have provided evidence for females in less closely
related pairs producing extra-pair offspring with more closely
related males.
To examine patterns of genetic compatibility, we studied the American redstart Setophaga ruticilla, a socially
monogamous Nearctic-Neotropical migratory bird with
relatively high rates of extra-pair paternity (43% of nests,
23% of offspring; Reudink et al. 2009a). Previous work on
extra-pair paternity in our study population in southeastern
Ontario, Canada, has revealed that males arriving early on
the breeding grounds are much less likely to lose paternity,
which provides possible support for the good genes hypothesis (Reudink et al. 2009a). Based on the genetic compatibility hypothesis, we predicted females that were more
closely related to their social partners would be more likely
to produce EPO compared to those less closely related to

2

their social partners. We also predicted that within broods,
EPO would be more heterozygous than WPO. Alternatively,
because this population has high rates of immigration
(Wilson et al. 2017), outbreeding may represent a higher
cost than inbreeding. Under this scenario, females less
closely related to their social partner would be more likely to
produce EPO and that, within broods, EPO should be less
heterozygous than WPO. Finally, we asked whether body
size and timing of arrival and breeding were associated with
adult heterozygosity. We determined relatedness of social
parents and heterozygosity of offspring by analyzing blood
samples of parents and offspring over eight years.

Material and methods
We studied a population of American redstarts from May–
July 2004 to 2011 at the Queen’s Univ. Biological Station in
southeastern Ontario, Canada (n = 106 nests, 414 nestlings;
mean nestlings per nest = 3.8 ± 1.2 SD). Details of all field
methods are described in Reudink et al. (2009a). Briefly,
birds were monitored and territories mapped throughout the
breeding season; plots were monitored throughout the arrival
period and adults were captured in mist-nets using decoys
and conspecific playback, at which time we took a 15–20 µl
blood sample by piercing the brachial vein. Each individual
was banded with a Canadian Wildlife Service-issued aluminum band and 2–3 colour bands and we took standard
measurements of tarsus length, tail length, unflattened wing
chord length, and body mass. For nestlings, blood samples
were taken on day 5 after hatching or on the day of fledging. No pairs were the same in multiple years; however, we
accounted for the fact that some females (n = 13) and males
(n = 20) were present in two years; no females were present
in more than two years, but four males were present in more
than two years.
Paternity analysis was conducted using five highly variable
microsatellite loci (Dpm01, Dpm03, Dpm05, Dpm15, and
Dpm16; 13–29 alleles per locus; see Table 1 in Reudink et al.
2009a) originally isolated from yellow warblers Setophaga
petechia (Dawson et al. 1997). For details on paternity analysis and assignment see Reudink et al. (2009a). To determine
relatedness between all social pairs, we used the R package
'related' (Pew et al. 2015). Using this package’s simulation
function, we compared four relatedness estimators by using
the allele frequencies of our population to generate 100
simulated pairs in each of the following categories: parentoffspring, full-siblings, half-siblings, and unrelated individuals. We determined that Wang’s relatedness estimate (Wang
2002) provided the highest correlation coefficient between
observed and expected relatedness estimates and thus was used
as our measure of relatedness. Note that due to the low success of assigning paternity to specific extra-pair males and the
presence of multiple extra-pair sires at nests (Reudink et al.
2009b), we were not able to directly compare relatedness of
extra-pair sires to within-pair males. However, because social

Table 1. Results from linear mixed models comparing heterozygosity of extra-pair offspring (EPO, n = 116) to within-pair offspring (WPO,
n = 298). Nest ID nested within female ID was used as a random effect in all models.
Variable
Difference in internal relatedness (IR) between within-pair and extra-pair offspring
Intercept
EPO versus WPO
Difference in standardized heterozygosity (SH) between within-pair and extra-pair offspring
Intercept
EPO versus WPO
Difference in homozygosity by loci (HL) between within-pair and extra-pair offspring
Intercept
EPO versus WPO

pair relatedness was strongly associated with the heterozygosity of within-pair young (r294 = 0.30, p < 0.0001), we felt that
extra-pair offspring heterozygosity could act as a useful proxy
for inferring relatedness of females and extra-pair sires.
We used the R package 'Rhh' (Alho et al. 2010) to analyze individual genotype data to determine three parameters
describing offspring heterozygosity: internal relatedness (IR),
standardized heterozygosity (SH) and homozygosity by loci
(HL). IR is a measure of heterozygosity that allows the frequency of each allele to contribute to the calculated value
so that rare shared alleles will produce higher values than
shared common alleles (Amos et al. 2001). This measure also
provides an estimate of relatedness between an individual’s
parents (Bean et al. 2004). High levels of heterozygosity are
indicated by negative IR values while high levels of homozygosity are indicated by positive values. SH provides a standard scale to measure heterozygosity for all individuals, and
is calculated by dividing the proportion of heterozygous loci
by the average heterozygosity of that locus (Coltman et al.
1999). Unlike IR, all loci equally contribute to the calculated SH value despite their allelic frequencies, and higher
SH values indicate higher heterozygosity. HL determines the
weight given to each locus by considering the allelic variability at each locus, so loci with less variability and more
alleles contribute more to the calculated value (Aparicio et al.
2006). Higher HL values indicate lower heterozygosity and
vice versa. This index was developed to accurately predict
heterozygosity in open populations with high levels of immigration; because IR gives more weight to rare shared alleles
and thus may underestimate the heterozygosity of offspring
of a native and an immigrant individual carrying rare alleles,
(Aparicio et al. 2006).
To ask whether the relatedness of social pairs whose nests
contained extra-pair offspring differed from those that contained only within pair offspring, we constructed a linear
mixed effects model using the Wang relatedness value as a
response, presence or absence of extra-pair offspring as a
main effect, and female ID as a random effect. We also asked
whether relatedness predicted the proportion of within-pair
offspring in a nest by constructing a model with proportion
of extra-pair offspring as a response, Wang relatedness as a
main effect, and female ID as a random effect. Next, we asked
whether relatedness of social pairs predicted reproductive

Estimate

SE

t

p

0.15
0.04

0.02
0.01

9.19
2.69

<0.0001
0.008

0.95
−0.04

0.02
0.02

49.7
−2.42

<0.0001
0.02

0.25
0.03

0.01
0.01

17.56
2.68

<0.0001
0.0008

success by creating three generalized linear models with
Poisson error distributions and a log link functions, using
number of eggs, number of nestlings or number of fledglings
as a response variable, Wang relatedness as a main effect, and
female ID as a random effect. Finally, to ask whether the heterozygosity of extra-pair offspring differed from within-pair
offspring, we constructed three linear mixed models using
heterozygosity (IR, SH or HL) as a response variable, extrapair/within-pair as a main effect and nest ID nested within
female ID as a random effect. We asked whether adult heterozygosity (IR, SH or HL) was associated with body size
(mass, wing, tarsus, tail) and arrival date (males) and first-egg
date (females) using Spearman’s ρ. To avoid pseudoreplication, each individual was only included once in the analysis
(most recent occurrence).
Data deposition

Data available from the Dryad Digital Repository: <http://
dx.doi.org/10.5061/dryad.96n24g7> (Hajdasz et al. 2019).

Results
Overall, we detected extra-pair offspring in 47/106 (44.3%)
nests, which accounted for 116/414 (28%) offspring in the
study. In nests containing EPO, the number of EPO ranged
from 1 to 4 (mean ± SD = 1.97 ± 1.10 EPO). We found no
difference in the relatedness of social pairs that produced only
within-pair offspring (n = 59 pairs; relatedness: 0.05 ± 0.03
SD) compared to social pairs whose nests contained extrapair offspring (n = 47 pairs; relatedness: 0.09 ± 0.03 SD)
(F1,87.8 = 1.72, p = 0.19). Similarly, there was no relationship
between proportion of within-pair offspring in a nest and
relatedness of the social pair (F1,95.2 = 0.08, p = 0.77). In addition, there was no relationship between the relatedness of the
social pair and number of eggs laid (n = 80 nests, z = 0.55,
p = 0.58), number of nestlings (n = 103, z = 1.21, p = 0.23), or
number of fledglings (n = 103, z = 0.85, p = 0.40).
We found that EPO had higher internal relatedness (IR),
lower standardized heterozygosity (SH) and higher homozygosity (HL) than WPO (Table 1). These results suggest
that females were more genetically similar to extra-pair than
within-pair mates, resulting in less heterozygous EPO.

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We found no associations between any measure of male
heterozygosity and tarsus length (all p > 0.37), tail length (all
p > 0.33), wing length (all p > 0.88), mass (all p > 0.12), or
arrival date on the breeding grounds (all p > 0.25). Similarly,
no measures of female heterozygosity were associated with
body size: tarsus length (all p > 0.36), tail length (all p > 0.33),
wing length (all p > 0.55), mass (all p > 0.44), first-egg date
(all p > 0.54).

Discussion
We found no evidence that females were more likely to produce extra-pair offspring based on relatedness to their social
mate. However, all three measures of heterozygosity indicated
that extra-pair offspring were significantly less heterozygous
than within pair offspring (Table 1). This finding suggests
that female American redstarts may be mating with extrapair males that are more genetically similar to themselves
than their social mates. These results contrast with several
studies demonstrating that extra-pair offspring are more heterozygous than within-pair offspring: e.g. blue tits Cyanistes
caeruleus (Foerster et al. 2003), superb starlings Lamprotornis
superbus (Rubenstein 2007), tree swallows Tachycineta
bicolor (Stapleton et al. 2007), and reed buntings Emberiza
schoeniclus (Suter et al. 2007). However, this pattern is not
universal as other studies on reed buntings (Kleven and
Lifjeld 2005), blue-footed boobies Sula nebouxii (Kiere et al.
2016), black-throated blue warblers Dendroica caerulescens
(Smith et al. 2005), and white-rumped swallows Tachycineta
leucorrhoa (Ferretti et al. 2011) have found no difference in
heterozygosity among extra-pair and within pair offspring.
Fewer studies have shared our findings of lower heterozygosity in extra-pair offspring; however, Kleven et al. (2005)
found North American barn swallow Hirundo rustica erythrogaster females were more genetically similar to their extrapair partners than social mates and that extra-pair young were
marginally significantly less heterozygous than within pair
young. These inconsistent findings may be partially due to
differences in methodology, as a meta-analysis of 43 studies
found an overall positive relationship between genetic similarity of social pairs and probability of extra-pair paternity,
but that only studies using microsatellite markers produced
a positive effect size (Arct et al. 2015). The authors suggested
that the level of outbreeding in a population could be an
important confounding variable in studies on pair relatedness
and extra-pair paternity.
One reason females may mate with more genetically
similar extra-pair males could be to avoid outbreeding depression (reviewed by Pusey and Wolf 1996). Negative effects of
outbreeding can arise due to the displacement of co-adapted
gene complexes or genes coding for local adaptations (Price
and Waser 1979, Frankham 1995). In general, the optimal
level of outbreeding is achieved by mating with distant relatives and avoiding mating with the closest relatives (Bateson
1978); for instance, female Japanese quail Coturnix japonica

4

prefer to mate with cousins over brothers or unrelated males
(Bateson 1982). As such, in highly outbred populations, we
may predict that females paired to highly dissimilar males
may be more likely to produce extra-pair offspring and do
so with more genetically similar males, resulting in extra-pair
offspring having lower heterozygosity.
Our population of American redstarts has extremely high
immigration rates, especially among males (Wilson et al.
2017), suggesting the possibility of an outbred population.
One prediction that arises from studies on potentially outbred populations that similarly found evidence of females in
less closely related pairs producing extra-pair offspring with
more closely related males (Rätti et al. 1995, Barber et al.
2005, Huyvaert and Parker 2010) is that less related social
pairs should also experience reduced reproductive success
(i.e. a cost associated with outbred pairings). We found no
evidence of this effect: relatedness of pairs was not associated with number of eggs, nestlings, or fledglings. Similarly,
we found no relationship between adult heterozygosity and
body size or arrival date/first-egg date, suggesting that, at least
in adults, any potential costs associated with high heterozygosity in this population are more subtle than these coarse
metrics. Overall, we demonstrated that extra-pair offspring
in our population of American redstarts are significantly
more homozygous than within-pair offspring, suggesting
that females are producing extra-pair offspring with more
genetically similar extra-pair partners, possibly to prevent
outbreeding depression.
Acknowledgements – We thank the many field assistants and
researchers that conducted field work on this project. We gratefully
thank C. Scott for assistance on molecular work and H. Taylor for
statistical and analytical advice.
Funding – Funding for this project was provided by the Natural
Sciences and Engineering Research Council of Canada (NSERC),
the Smithsonian Institution, Canadian Foundation for Innovation,
Ontario Innovation Trust, Sigma Xi, the American Ornithologists’
Union, the Canadian Society of Ornithologists, the American
Museum of Natural History and the National Science Foundation.
Permits – Research was conducted under Queen’s Univ. Animal
Care and Use Committee guidelines and under Canadian Wildlife
Service collection permit no. CA 0154 and banding permit
no. 10766C.

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