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Animal Behaviour 79 (2010) 261–264
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/anbehav
Low level of extrapair parentage in wild zebra finches
Simon C. Griffith a, b, *, Clare E. Holleley a, b, Mylene M. Mariette a, b, Sarah R. Pryke a, b, Nina Svedin a
a
b
Department of Brain, Behaviour and Evolution, Macquarie University
School of Biological, Earth and Environmental Sciences, University of New South Wales
a r t i c l e i n f o
Article history:
Received 28 September 2009
Initial acceptance 12 October 2009
Final acceptance 16 November 2009
Available online 7 December 2009
MS. number: 09-00639
Keywords:
extrapair paternity
intraspecific brood parasitism
sexual conflict
sexual selection
sperm competition
Taeniopygia guttata
zebra finch
The captive zebra finch, Taeniopygia guttata, has become one of the key vertebrate model systems for
studying a range of behavioural, physiological and neurological phenomena. In particular, this species has
played a key role in developing our understanding of sexual selection and sperm competition. In contrast
with the large number of studies using domesticated zebra finches, relatively few studies have focused
on free-living populations of wild zebra finches. Investigating the incidence of extrapair paternity in
zebra finches in the Australian desert, we found a very low level; 1.7% of 316 offspring from four of 80
broods fathered outside the pair bond. These numbers contrast with the high levels of extrapair paternity
observed in domesticated aviary populations, and suggest a low level of sperm competition and sexual
selection in natural populations. Our finding of such a low rate of extrapair paternity in the wild zebra
finch suggests that it is one of the most genetically monogamous of all passerine species and that has
important implications for future studies of this model organism in studies of sexual selection and
reproductive biology. In addition, we found that 5.4% of 316 offspring were not related to either putative
parent and hatched from eggs that had been dumped by intraspecific brood parasites.
Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
In birds, about 90% of all species form socially monogamous pair
bonds, and in these species 11% of offspring, on average, are sired by
an extrapair male (Griffith et al. 2002). Extrapair paternity (EPP) is
an important evolutionary phenomenon in socially monogamous
species because it can dramatically increase the variance in
reproductive success among males within a population (Whittingham & Dunn 2005), and it can provide an important postcopulatory mechanism for selection on genetic compatibility
(Griffith & Immler 2009). In addition to describing the variation in
the level of EPP and accompanying sexual selection across species,
research has focused on the physiological and behavioural
processes that relate to the incidence of EPP. Foremost among these
is sperm competition (Parker 1970), an area in which the zebra
finch, Taeniopygia guttata, has been one of the most widely used
model organisms because of its amenability as a captive animal.
Studies of the zebra finch represent a significant proportion of all
the empirical work contributing to our understanding of the
mechanisms of sperm competition in birds, including the timing
and frequency of pair and extrapair copulations (Birkhead et al.
1989), sperm precedence models (Birkhead et al. 1988b), fertilization success and sperm quality (Birkhead et al. 1993), sperm storage
* Correspondence: S. C. Griffith, Department of Brain, Behaviour and Evolution,
Macquarie University, Sydney, New South Wales 2109, Australia.
E-mail address: simon.griffi[email protected] (S.C. Griffith).
(Birkhead et al. 1989), sperm depletion and allocation (Birkhead &
Fletcher 1995), sperm morphology (Birkhead et al. 2005), and
female propensity to engage in extrapair copulations (Forstmeier
2007). The zebra finch has been similarly prominent in the field of
sexual selection through studies of mate choice (e.g. Rutstein et al.
2007), ornamental song (e.g. Collins et al. 1994), parental care (e.g.
Burley 1988), sex allocation (e.g. Burley 1981) and maternal effects
(e.g. Gil et al. 1999). All of these important and influential studies
have focused on domesticated birds that have been selectively bred
for over 100 generations (Zann 1996), and held in conditions that
are far removed from those experienced by free-living wild birds.
The use of domesticated model organisms is a crucial component of
modern biological research. However, to aid the interpretation of
captive studies it is important to develop an understanding of the
wild context from which the model organism originated. A
previous study of the zebra finch population studied over a long
period by R. Zann in Victoria, Australia (Birkhead et al. 1990) found
a very low level of EPP and intraspecific brood parasitism. However,
there are a number of currently unresolved issues arising from this
study. First, the study by Birkhead et al. (1990) was based on a small
sample of just 25 families situated on an irrigated farm in
temperate Victoria, which bred at very low density and synchrony
and may not have truly represented the species in its native environment (T. R. Birkhead, personal communication). Furthermore,
Birkhead et al. (1990) reported a potential case of quasiparasitism
from families in which the molecular methods used were unable to
0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2009.11.031
262
S.C. Griffith et al. / Animal Behaviour 79 (2010) 261–264
make an accurate discrimination of the level of relatedness to
a brood parasite and the pair male simultaneously (see Griffith et al.
2004). Here therefore for the first time we investigated the level of
EPP in wild populations of free-living zebra finches breeding in
their natural arid zone environment in Australia.
METHODS
Sampling of Wild Populations
Between August 2005 and December 2007, we monitored 572
breeding attempts in nestboxes at four localities at the Fowlers
Gap Arid Zone Research Station in far-west New South Wales,
Australia (31050 S, 142 420 E; details in Griffith et al. 2008).
Nestlings were banded before fledging and a small blood sample
(<20 ml) was taken from the brachial vein. Adults were caught
using nestbox traps that were watched and birds removed at the
time of capture. All adults were blood sampled (<20 ml) and
banded with a numbered aluminium band and either a unique
combination of colour bands or a transponder tag (11 mm long
and 2 mm wide and 0.1 g, Trovan ID100) attached to a plastic
colour band. Putative parents were either captured while feeding
nestlings, or later confirmed to have revisited the same nestlings
through direct observation or remote reading of the transponder
tag. We selected 80 complete families for a molecular survey to
represent the different years of study and the different areas
within the site. To estimate the opportunity for females to
engage in extrapair copulations (EPCs), for each sampled pair, we
counted the other reproductively active pairs (i.e. eggs or chicks
present in the nest) within 1 km of their nest during the egglaying period of the focal female. This work was conducted under
the authorities of the Animal Ethics Committees at the University
of New South Wales and Macquarie University, a Scientific
Research Permit from the New South Wales Parks and Wildlife
Service and a banding Authority of the Australian Bird & Bat
banding Scheme.
Molecular Methods
We used six fluorescently labelled microsatellite loci (Tgu1,
Tgu3, Tgu8, Tgu10, Tgu12, Tgu4) that had previously been isolated
and characterized in this species (Forstmeier et al. 2007) and
a sex identification locus (Griffiths et al. 1998) in two multiplex
PCR reactions that were designed with the program Multiplex
Manager 1.0 (Holleley & Geerts 2009). Fragment size analysis
for all seven loci was conducted concurrently in a single run on
a 48-Capillary 3730 DNA Analyser (Applied Biosystems, Foster
City, CA, U.S.A.), and conducted using GeneMapper version 3.7
(Applied Biosystems). There was some amplification failure but
individual samples were rerun to ensure that each individual was
scored with at least five of the six microsatellite loci. The overall
final amplification failure rate of each locus was 0.21–3.33%,
which given the frequency of null alleles is possibly due to a low
number of individuals carrying two null alleles at a particular
locus.
In the 169 presumably unrelated adults genotyped, the loci were
all highly variable with an average of 34 alleles per locus (range
22–42). The combined nonexclusion probabilities calculated by
CERVUS 3.0 (Kalinowski et al. 2007) for this set of markers in this
population were P ¼ 0.00008 for the first parent and P < 0.00001
for the second parent. Because of the characteristics of the genetic
markers in this population, all offspring could be readily assigned
unambiguously to their putative parents (or excluded) based on
shared or mismatched alleles.
RESULTS
Of 316 offspring, 17 (5.4%) from 14 of 80 broods (17.5%) were not
related to either parent and hence were the result of intraspecific
brood parasitism (IBP; Tables 1, 2). In each of three broods two
chicks resulted from IBP and in all three cases these two dumped
chicks were unrelated to each other (with no more than one allele
matching across the six multisatellite loci) and hence must have
resulted from two different parasitic females. We found no case of
quasiparasitism. Of the remaining 299 offspring, five (1.7%) from
four of 80 broods (5.0%) were sired by an extrapair male (Table 1).
Multiple mismatching loci were used to exclude all offspring
resulting from EPP or IBP. Although mismatch with the putative
father or mother occurred at a single locus in 26 offspring, all these
mismatches can be explained by allelic dropout (i.e. the offspring or
parent was a homozygote and therefore the mismatched alleles are
likely to have simply failed to amplify during the molecular
procedure). In addition, given the high level of allelic diversity and
frequencies of the different alleles, it is implausible that another
individual could have been responsible and matched the offspring
by chance at five of the six loci. Furthermore, all of the offspring
that mismatched their parents at multiple loci mismatched
consistently at between four and six of the loci used (average
number of mismatched loci ¼ 5.18). All 80 families were sampled
during the main breeding season and focal birds nested in close
proximity to other breeding birds with each pair having an average
of 18 other actively breeding pairs within 1 km radius of their nest
(with at least twice as many nonbreeding adults around),
presenting ample opportunity for EPC (Table 1).
DISCUSSION
Wild zebra finches breeding in the Australian desert had a very
low level of EPP (1.7% offspring in 5% of broods), suggesting that the
zebra finch is among the most genetically monogamous bird
species surveyed to date (Griffith et al. 2002). By contrast, in
a captive population of 30 pairs of ‘wild-type’ North American
domestic zebra finches living in a single aviary (53 m3), Burley et al.
(1996) found that 28% of 278 offspring in 37% of 126 broods were
fathered by an extrapair sire, a level of EPP that would put the
species in the upper quartile with respect to variation in the level of
extrapair fertilization.
The difference in the rate of EPP between the free-living wild
birds and the captive population of domesticated birds could be
caused by social or environmental factors or possibly by artificial
selection imposed by aviculturists for over 100 generations. Given
Table 1
The incidence of extrapair paternity (EPP) and intraspecific brood parasitism (IBP)
among families in four different areas across 3 different years with the average
number of pairs actively breeding in those areas at the time of the sampled reproductive attempt
Area
Year
No. of
broods
No. of
broods
with EPP
East Mandelman
West Mandelman
West Mandelman
Gap Hills
Gap Hills
Gap Hills
Saloon
Saloon
Saloon
2005
2005
2006
2005
2006
2007
2005
2006
2007
15
7
3
12
14
19
7
2
1
0
1
1
0
1
1
0
0
0
1
0
0
3
2
4
4
0
0
80
4
14
Total
No. of
broods
with IBP
No. of pairs
within 1 km
(average)
18
23
7
25
13
40
15
7
17
18.33
S.C. Griffith et al. / Animal Behaviour 79 (2010) 261–264
Table 2
The incidence of extrapair paternity and intraspecific brood parasitism across broods
of different size
Brood size
Total no. sampled
No. of broods
with EPP
No. of broods
with IBP
1
2
3
4
5
6
1
7
24
22
15
11
0
0
2
2
0
0
1
1
1
2
5
4
that males apparently court females for EPC at a similar rate in
captive and wild populations (Birkhead et al. 1988a; Burley et al.
1994), the difference in rates of EPP may simply reflect differences
in female propensity to accept or reject EPC in the two contexts.
Domestic females appear to be less choosy than their wild
counterparts (Rutstein et al. 2007), and thus may be less likely to
resist EPCs.
The levels of both EPP and IBP found in our study of desert-living
birds were very similar to those reported previously for a wild
population on an irrigated farm in northern Victoria, Australia
(Birkhead et al. 1990). In their study, Birkhead et al. (1990) found
that two of 82 offspring (2.4%) were extrapair, in two of 25 broods
(8%), and that 10 offspring (11%) from nine of 25 broods (36%)
hatched from eggs that were the result of IBP, one of which was
suggested to be the result of quasiparasitism (Birkhead et al. 1990;
Griffith et al. 2004). Our study increases the number of wild
families studied (from 25 to 105) and used a more ‘classic’ zebra
finch population, both in terms of habitat (the arid and semiarid
zone represents >80% of the zebra finch distribution) and the range
of breeding densities and synchronies, than the earlier study conducted in the nonarid zone on birds breeding at low density and
synchrony (Birkhead et al. 1990). The remarkably small difference
(0.7%) in the level of EPP found in these two studies conducted over
1000 km and 17 years apart suggests that we can now be fairly
confident that EPP in natural populations of the zebra finch is very
low, accounting for only 1–2% of offspring (the combined rate of
EPP from both wild studies is 1.7% (95% confidence interval
0.5–3.0). Although extrapair courtship and copulations do occur in
the wild (Birkhead et al. 1988a), this low level of EPP suggests that
sperm competition is likely to be limited, with social partners
acquiring most fertilizations, probably because of the combined
effects of female resistance and the timing and rates of extrapair
and within-pair copulations (Birkhead et al. 1988a, b, 1989).
The zebra finch has provided a good model for investigating the
components of avian reproductive biology that were essential in
the development of a mechanistic understanding of the process of
sperm competition. For example, work on the captive zebra finch in
Europe has helped to demonstrate the role of the sperm storage
tubules in avian reproduction (Birkhead et al. 1993) and the
fact that a passive loss model (of sperm from the female reproductive tract), coupled with the difference in ejaculate size between
males, can explain why the last male to copulate with a female
typically fertilizes the majority of the eggs (Birkhead et al. 1988b;
Colegrave et al. 1995). It would not have been feasible to conduct
the necessarily controlled experiments that led to such findings on
wild birds, and therefore the zebra finch was probably the only
passerine that could have been the focus of such a study.
However, a more recent study of sperm design probably reflects
a situation in which, by being an inappropriate model, the zebra
finch initially caused confusion rather than clarity. In their study,
Birkhead et al. (2005) used a large pedigree of 1526 individuals to
investigate the source and consequence of variation among males
in the morphology of their sperm (again something that would be
263
difficult to achieve in an alternative avian model system). A
considerable amount (relative to standard morphological traits) of
intermale variation was found with respect to sperm design and
these traits were all highly heritable (Birkhead et al. 2005). The
paradox here is that we should not expect to find so much variation
in traits that are closely associated with fitness and under such
a high level of genetic control. The low level of EPP that we have
demonstrated here helps to put the earlier study (Birkhead et al.
2005) of sperm design into context. As males are rarely exposed to
selection on the ability of their sperm to swim faster than sperm
from other competing males then it is not too surprising that lots of
morphological variation in sperm design exists in populations of
zebra finches. Further comparative study has indeed revealed that
the level of intermale variation in sperm morphology is much lower
in species with higher levels of EPP than the zebra finch (Kleven
et al. 2008). By contrast, in species in which offspring are regularly
produced by EPP and thus where there is a high incidence of sperm
competition, the sperm produced by males across a population
exhibited greater similarity of form and presumably reflected
a more tightly selected optimum for competing within the female
reproductive tract (Kleven et al. 2008).
The zebra finch has thus provided a good model system for
understanding the fundamental reproductive biology of passerine
birds but may not be such a good system for understanding the way
that the selection driven by EPP (which occurs at a significantly
higher rate in most other birds) affects morphology, behaviour and
physiology.
Our findings in the wild zebra finch have important implications
for the use of this species as a model system in a more general sense
(than in sperm competition). In socially monogamous species, EPP
can be an important driver of sexual selection and sexual conflict,
because it can increase the variance in reproductive success among
individuals (Whittingham & Dunn 2005) and create disparity
between the evolutionary interests of the male and female,
respectively. Given that wild zebra finches form pair bonds that are
maintained throughout the year and apparently last until the death
of one partner (Zann 1996), the low level of EPP we observed
suggests that this species more closely approaches true monogamy
than most other birds; thus there may be relatively little sexual
conflict. If most individuals in wild populations remain genetically
monogamous then most sexual selection will be on the reproductive success of pairs rather than individuals, and therefore the focus
of research in this species should perhaps be placed on parenting
behaviour and the ability of individuals to bond, synchronize and
reproduce effectively with their partner. In contrast however, over
the past couple of decades much of the research in this species has
investigated conflict between the male and female partner (e.g.
Burley 1988; Gil et al. 1999; Royle et al. 2002). It is important to
stress that we believe that sexual conflict and sexual selection do
occur in this species; indeed the study by Royle et al. (2002) is one
of the clearest demonstrations of sexual conflict in any vertebrate,
while many studies have demonstrated active choice of social
partners (e.g. Rutstein et al. 2007).
Like many of those who have worked on captive zebra finches,
we agree that the zebra finch is a good model system to study
because of its amenability to highly manipulative and controlled
experiments. However, we suggest that caution is used when trying
to infer general conclusions from studies relating to sexual selection and sexual conflict in this species. Rather than representing the
‘average’ socially monogamous bird, the zebra finch may instead
represent the less interesting end of avian biodiversity in relation to
sexual selection, sexual conflict and sperm competition and it is
likely that there are more extreme, more complex and more
interesting processes occurring in other avian species with respect
to each area of study.
264
S.C. Griffith et al. / Animal Behaviour 79 (2010) 261–264
Acknowledgments
We thank James Brazill-Boast, Gareth Davies, Richard Merrill,
Emma Pariser, Ian Stewart, Ingrid Stirnemann, Harriet Stone and
Megan Taylor for assistance in the field; Wolfgang Forstmeier for
providing access to unpublished primers; and Wolfgang Forstmeier
and Jan Lifjeld for useful comments on the manuscript. S.C.G., C.E.H.
and S.R.P. were supported by the Australian Research Council,
M.M.M. by a Macquarie University Research Excellence Scholarship,
and N.S. by a Postdoctoral Fellowship from the Swedish Research
Council (Vetenskaprådet).
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