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Behavioral Ecology Vol. 11 No. 3: 265-273
© 2000 International Society for Behavioral Ecology
High fidelity on islands: a comparative study of extrapair paternity in passerine birds
Department of Evolutionary Biology, EBC, Uppsala University, Sweden
Address correspondence to S. C. Griffith, Department of Evolutionary Biology, EBC, Uppsala University, Norbyvägen 18D, S-752 36 Uppsala, Sweden. E-mail: simon.griffith{at}zoologi.uu.se .
Received 8 April 1999; revised 25 July 1999; accepted 24 August 1999.
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ABSTRACT |
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It is commonly assumed that the intensity of sexual selection is lower in island populations. Extrapair paternity (EPP) is widespread within passerine birds and is indicative of sexual selection. A conservative analysis of the levels of EPP in island and equivalent mainland populations of passerines reveals that insular populations are indeed characterized by low levels of EPP. This supports the idea that the intensity of sexual selection is lower on islands. This relationship has previously been predicted, based on the assumption of low levels of genetic variation for fitness in such populations. The evidence from this analysis suggests that this is just one of several nonmutually exclusive hypotheses that may explain the high fidelity of island-living females.
Key words: extrapair paternity, island populations, passerines, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The discovery that extrapair paternity (EPP) is a widespread feature of the most common avian mating systems has revolutionized our understanding of sexual selection in birds. Revealing the causes of the observed variation in the reported levels of EPP in different species and populations will be critical to fully understanding the mechanisms driving extrapair behavior (Petrie and Kempenaers, 1998
).
If EPP is the result of a female's propensity to participate in extrapair
copulations (EPCs) (given that willing males are available), then variation in
the level of EPP will be determined largely by the costs and benefits of EPCs
to females. The observed level of EPP in natural populations shows great
variation, from 0% (e.g., Gyllensten et
al., 1990) to >75% (Mulder
et al., 1994). Several factors have been suggested to account for
this variation at both the species and population level. For example, the
breeding system—from social monogamy through polygyny and polyandry to
cooperative breeding systems—will obviously have a profound effect on
the female cost-benefit relationship of engaging in EPCs. The precise nature
of such effects is unclear and will undoubtedly be confounded by life-history
variables such as annual fecundity of individuals and life span
(Birkhead and Møller,
1992).
Other, more subtle variables, which may differ between species but also
between populations of one species, will also affect the level of EPP. It has
been suggested that the level of EPP will be positively related to both the
local breeding density (Møller and
Birkhead, 1993) and degree of breeding synchrony within
populations (Stutchbury and Morton,
1995). Both of these ideas are still controversial, and clear
support for both ideas is lacking (e.g., see
Westneat and Sherman, 1997;
Weatherhead and Yezerinac,
1998).
Petrie and Lipsitch (1994)
proposed that the degree of polygyny will be related to population levels of
variation for fitness-related genes. The degree of polygyny could be viewed
synonymously with the level of EPP, with some males likely to be mated to
multiple females. A comparative analysis of the levels of allozymic variation
in species with differing levels of EPP supports the predictions of the model
(Petrie et al., 1998);
however, in their analyses there is some difficulty in establishing cause and
effect. Additionally, this theory relies on the assumption that EPP is largely
caused by females seeking good genes—an idea that currently has received
little direct support (but see Hasselquist
et al., 1996; Sheldon et al.,
1997). Other studies have demonstrated that EPP may result from
females seeking direct benefits (e.g.,
Gray, 1997).
Generally, there are two nonmutually exclusive groups of populations, which
may be expected to have a below average level of genetic diversity, allowing
an indirect test of this hypothesis. The first is those populations that have
historically been through a genetic bottleneck due to a significant numerical
decline, often due to human pressure. The second is naturally occurring
island-dwelling populations, which are expected to exhibit low levels of
genetic variation due to a combination of founder effects, inbreeding, genetic
drift, and low rates of dispersal
(Jaenike, 1973;
Wright, 1931). Frankham
(1997) found that, like other
taxa, island-dwelling populations of birds do indeed have lower levels of
genetic variation (measured with allozymes, nuclear DNA markers, and
mitochondrial inversions) than those living on larger landmasses. On this
basis, a comparative analysis of EPP in island and mainland populations of
birds will test the expectation of Petrie and Lipsitch
(1994) that island populations
will exhibit significantly lower levels of EPP.
If island populations do exhibit lower levels of EPP, then the implications
are potentially great for some of the classic evolutionary studies which have
focused on island populations of passerines, as well as recent studies (e.g.,
Grant, 1986;
Komdeur, 1996;
Smith, 1988). Extrapair
paternity is a common and widespread behavior in avian breeding systems
(Petrie and Kempenaers, 1998)
and will play a significant role in sexual selection within such systems. If
such an important component of the avian breeding system is insignificant in
island populations, then they must be abnormal in some fundamental way, and
the use of island systems to study mating systems must surely be
questioned.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Data set
Extrapair paternity is widespread and shows great variation in the Passeriformes (Petrie and Kempenaers, 1998
), a homogeneous group well enough represented in the
literature to enable a test of whether island populations do exhibit low
levels of EPP through the comparative approach. I have followed Westneat et
al.'s (1990) definitions of
pair-bonds and EPP; thus a pair-bond is viewed as an extended social and
sexual association between a male and female, lasting considerably longer than
the time taken to copulate. Subsequently, EPP can result from a mating between
a female and a male other than her pair-bonded mate. This definition excludes
copulations between females and males that have extensive social associations
such as, for example, a multiply mated female in a polyandrous breeding system
(e.g., the mating system of the dunnock, Prunella modularis;
Burke et al., 1989).
Cooperative breeding is defined as a reproductive system in which one or more
members of a social group of more than two adults provide care to young that
are not their own (Stacey and Koenig,
1990). For cooperative breeders, EPP is actually extragroup
paternity; however, for simplicity it will also be referred to as EPP.
I compiled data on levels of EPP from original sources that were located by
searching the major biological and ornithological journals and searching the
BIDS and BIOSIS databases. All published studies (up to the end of January
1999) that have reported the level of EPP in wild, unmanipulated populations
based on reliable genetic techniques (multi- or single-locus minisatellite
fingerprinting or polymerase chain reaction-based microsatellite genotyping)
were included. I omitted studies based on allozymes, plumage markers, and sex
differences in heritability estimates due to their poor precision and the
ambiguity of such results with regard to the difference between EPP and
intraspecific brood parasitism (see
Westneat and Sherman, 1997).
There is no reason to suspect that the exclusion of these results caused
consistent bias with regard to the hypothesis being tested.
To be applicable to the hypothesis of Petrie and Lipsitch
(1994), an island population
should ideally conform to both of the following characteristics: (1) the
population should be sedentary on the island throughout the year. Those
species that breed on an island but are migratory cannot reasonably be
expected to suffer reduced genetic variation because vagrants are likely to
immigrate into the breeding population. Similarly, the population must be
effectively isolated from wintering conspecifics. (2) The island must be
reasonably small so as not to contain too large a population. Fundamental to
the idea of reduced genetic variation within an island population is the
effective population size. This will be related to the size of the island via
the ecological carrying capacity and also to the spatial distribution of
individuals within that population. A landmass such as Britain, which has been
classed as an island by some authors (e.g.,
Fitzpatrick, 1998), obviously
cannot realistically be classified as an island with respect to the hypothesis
in question.
Although it may appear that the definition of what constitutes an island appears subjective, in this data set there is a clear distinction between island and nonisland populations. Size is potentially the most arbitrary category, and in this data set there is a considerable difference between the smallest piece of land classified as mainland (Britain 244,820 km2) and the largest island (Gotland, Sweden; 57° N, 18° E, 3170 km2; see Figure 1). Finally, although small patches of suitable habitat within a larger land mass may represent islands to certain species, I did not account for such situations in this study due to the obvious difficulty in detecting and defining such ecologically delimited islands.
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Analysis
The data set consists of 74 populations from 54 different species. Eight of
the populations in the data set are cooperatively breeding species, which were
excluded from the main analysis because EPP is likely to be affected by
different factors in such breeding systems. Of the remainder, 13 of the
populations live on islands and 53 live on larger land masses. For species in
which the level of EPP had been estimated in more than one population, I
calculated a mean for the species based on all the populations within one of
the two categories (either island or mainland), weighted by sample size of the
component estimates.
The hypothesis can be tested using a simple comparison of the mean level of
EPP in the island populations with the mean level in the mainland populations.
The validity of this test relies on the independent derivation of the island
state. The phylogeny of the order is presented in
Table 1, and from the
distribution of island populations it seems most parsimonious that the island
state is in fact independently derived for each of these populations. In
addition, only three of the species are island endemics with most species
living both on islands and mainland and therefore island living is not a
species characteristic. Although for the above reasons it is unnecessary to
control for the effects of nonindependent derivation of island populations, to
be conservative I repeated the analysis using a pairwise analysis of closely
related species or populations (following
Møller and Birkhead,
1992). For each pairwise comparison I paired the island population
with the mainland population most closely related to it using the
molecular-based phylogeny of Sibley and Alquist
(1990) (see Table 2). In each
case pairs were constructed with species from the same tribe or subfamily. Two
island populations could not be paired (Petroica australis and
Zosterops lateralis), as they are the only members of their
respective families subjected to genetic parentage studies. The exclusion of
these two can only make the analysis more conservative, as the level of EPP in
both was found to be 0%, and therefore it is impossible for a comparative
population to have a lower level. Four of the 10 pairs are intraspecies
comparisons, which is the best test of the hypothesis. Finally, as discussed
above, to conform to the idea of Petrie and Lipsitch
(1994), island populations
should be closed to excessive, regular gene flow, and therefore species that
breed on islands but migrate to them annually should be excluded from the
analysis. Four of the 10 island populations are migratory, and therefore I
repeated the analysis with these pairs excluded.
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For all the above comparisons mean levels of EPP were established from the available data (again weighted for sample size), and the pairs were analyzed using the nonparametric paired Wilcoxon test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The mean level of EPP in island-dwelling populations of passerines was significantly lower than the level of EPP in populations living on larger landmasses (see Figures 2 and 3a). The mean level of EPP in island populations was 8.2% (±3.4 SEM) and in mainland populations was 17.6% (± 1.7
nn-Whitney, z = 2.52, n = 66,
p =.01; see Figure
3a).
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The pairwise comparison between island and equivalent mainland populations, which controlled for the possible non-independent derivation of the island state, confirmed this result (Wilcoxon z = 2.16, n = 10, p =.03; Figure 3b). In 8 of the 10 pairs, the island population had a lower level of EPP. Interestingly, the two island populations that did not conform to the overall relationship were the populations of the collared flycatcher and willow warbler, both on Gotland, the largest island in the data set and also both migratory species. As shown in Figure 3a, the four migratory island populations exhibit the highest levels of EPP within the island data set. This observation suggests that, as expected, the island effect does not apply to migratory species. If the analyses are repeated excluding these four migratory species, there is a significant difference between island and mainland species, even though the sample size is greatly reduced (Wilcoxon z = 2.81, n = 6, p =.005).
As shown in Figure 2, the accuracy of reported levels of EPP are dependent on the sample size of offspring used to construct the estimate. For illustrative purposes, the shaded areas on the graph represent the 95% and 99% confidence intervals around the mean level of all passerine populations (15.9% ± 1.6), across different sample sizes. As illustrated, the estimates of island populations are based on sample sizes equivalent to those of the mainland populations. The four island populations within the boundaries of the 95% confidence limits around the mean level of EPP for passerines are the four migratory species (see above); nearly all of the others (seven out of eight) are significantly lower than the mean level at the respective sample sizes. The single exception is an estimate of 0% based on a small sample of offspring.
Therefore, the above results are not unduly affected by a consistent bias in the unreliability of either island or mainland population estimates. In the pairwise comparative data there was no difference between the mean sample size used for island and mainland estimates of EPP (Wilcoxon z = 0.45, n = 10, p =.65). For 8 of the 10 pairs in the comparative analysis there are estimates of breeding density for both the island and mainland populations (see Table 1). In five cases the island populations bred at a higher density, whereas in the other three the mainland populations bred at higher density, but in most cases the differences were not great. There is no significant difference between the breeding density of the mainland and island populations used in this analysis (Wilcoxon z = 0.98, n = 9, p =.33). Most convincingly, the differences between the breeding densities of the island and mainland populations of the four species that are represented by both mainland and island populations (i.e., Parus major, P. caeruleus, Phylloscopus trochilus, and Passer domesticus) are negligible (see Table 1).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The finding that insular populations exhibit significantly lower levels of EPP than other populations is consistent with the model proposed by Petrie and Lipsitch (1994
). However,
there are several viable alternatives that are difficult to exclude. First,
the set of species or populations inhabiting islands today (and therefore
available to study) may not reflect a nonrandom set of all passerines. Such
populations may be present due to a characteristic in which suitability for an
insular existence covaries with a significantly lower-than-average level of
EPP. For example, Sorci et al.
(1998) found that, after
anthropogenic introduction to New Zealand, dichromatic species were more
likely to become extinct. The interpretation was that strong sexual selection
made a species less competitive and unable to force its way into a new
environment.
An alternative idea which may bear some relevance comes from the detailed
studies of speciation in Hawaiian Drosophila and is argued to be
responsible for asymmetric sexual isolation in species pairs on different
islands. It was suggested that, after a founder event, when a population is
still small, females are unable to satisfy all their mate choice requirements,
and this subsequently leads to a shift in the choosiness of females within
sister species pairs (Kaneshiro,
1976). In the given example of Drosophila, courtship
patterns are quite complicated, and it appears that only some parts of the
courtship are lost (Hoikkala and
Kaneshiro, 1993). It is possible that such founder effects may
lead to a reduction in the choosiness of females even in species in which
courtship is more simple or based primarily on one or two simple traits,
particularly if there are costs associated with female choosiness. Either of
these two routes of selection may have led to differences between the island
populations and mainland populations used in this analysis. However, with our
present limited knowledge about the extent of genetic variation for both
female choosiness and promiscuity in birds, it is difficult to predict the
importance of such effects. It is also hard to imagine how such processes
could account for such significant differences between populations of the same
species (e.g., Passer and Parus), particularly where gene
flow is not restricted (Griffith et al.,
1999; Verhulst and van Eck,
1996).
An alternative to differences between populations caused by selection is
the idea that the observed differences between island and mainland populations
are the result of phenotypic plasticity in response to the island environment.
For example, a female in an island environment may be less likely to seek EPCs
than a female in a mainland population. It is not known whether such
differences are due to selection or environmental determination (or a
combination of both), but several studies have revealed systematic differences
between island-dwelling birds and their mainland counterparts. Male coloration
has been shown to be drabber on islands
(Fitzpatrick, 1998), and
island and mainland populations show divergence in many reproductive traits.
For example, great tits on offshore islands in Denmark bred later, laid
smaller clutches, and laid larger eggs than those on the mainland
(Wiggins et al., 1998). Low
genetic diversity, lower food abundance, and density dependence were given as
possible reasons for these differences in the reproductive ecology of the
different populations.
The evidence for lower genetic variation of island versus mainland
populations is quite clear. Island populations of mammals, birds, reptiles,
insects, and plants had 29% lower heterozygosity compared with mainland
populations of the same species (Frankham,
1997). This gives some support to the idea that low genetic
variation may lead to reduced levels of EPP through the route proposed by
Petrie and Lipsitch (1994);
however, this interpretation should be drawn with caution. Petrie and
Lipsitch's (1994) theory
concerns additive genetic variance for traits related to fitness, but most
estimates of genetic variation are based on allozyme studies and studies of
supposedly neutral genetic markers. There is some discussion of the extent to
which allozyme heterozygosity correlates with additive genetic variation for
traits related to fitness (Butlin and
Treganza, 1998), and, indeed, any relationship that does exist is
likely to be weakened by low effective population sizes
(Lande, 1988).
Several observations point to the fact that, in at least some cases, the
island effect is unlikely to be caused by low genetic variance. The level of
heterozygosity and allelic diversity at microsatellite loci in the island
population of house sparrows on Lundy off the southwest coast of England were
no different from that in several mainland populations. This observation was
in line with expectation, given the effective population size and the number
of immigrants per generation (Griffith et
al., 1999). Similarly, the population of great tits breeding on
Vlieland, an island in the Dutch Wadden Sea, is highly unlikely to be
genetically different from the mainland population, given that each year,
approximately 25% of the breeding females arrived on the island as immigrants
from mainland populations (Verhulst and
van Eck, 1996). Naturally, some of these island populations are
small, isolated ones that in some cases have been through substantial genetic
bottle-necks: for example, the study population of the New Zealand black robin
(approximately 150 pairs) was established from just 5 individuals
(Ardern et al., 1997).
Although the difference in genetic variation between island and mainland
populations appears to be a likely candidate for at least some of the observed
differences, there are some non-mutually exclusive alternatives that are
testable and require further investigation. Petrie and Lipsitch
(1994) focused on the
potential benefits to participation in EPCs, but the level of EPP will also
depend on the costs of EPP for females. For a socially monogamous passerine,
perhaps the greatest cost is the loss of male help in rearing offspring.
Monogamy is assumed to be so prevalent among passerines due to the constraints
of egg laying and the advantages of biparental care to the successful
production of offspring (Gowaty,
1996). Several studies have revealed a negative relationship
between a male's certainty of paternity and the proportion of food he brings
to the nest relative female provisioning (see
Wright, 1998). Given the
potential cost of such punishment to the female in terms of both current and
future reproduction, perhaps in a more ecologically constrained island
environment the costs are proportionally higher and not worth paying. This
idea could be tested by manipulating ecological aspects of island populations
to reduce the constraints and make them comparable to those encountered by
mainland populations.
Other characteristics of insular populations may also adjust the
cost—benefit equation for female participation in EPCs. For example,
Slagsvold and Lifjeld (1994)
proposed that EPP should be lower in populations or species in which females
can assess the quality of males over a long period. Perhaps in small, insular
populations individuals have good opportunity to thoroughly judge each other,
and therefore they will mate assortatively with respect to quality, resulting
in low levels of EPP. It is difficult to determine the extent to which this
idea may explain the difference between island and mainland populations in the
level of EPP. However, it is interesting that within island populations, those
with the highest levels of EPP were those that migrated to the breeding area
and only arrived a short time before pair formation.
Although breeding density may vary between mainland and island populations,
within a species this variation is apparently limited (certainly within this
data set), and there does not seem to be an overall trend for islands to have
either abnormally low or high breeding densities. In fact, in this data set
island populations are more likely to be of a higher density than
corresponding mainland populations. This leads to an expectation of higher
level of EPP (Westneat and Sherman,
1997) on islands and therefore suggests that the island effect is
stronger than any density dependence of EPP. Certainly, any affect of islands
on EPP is unlikely to be caused by the effects of breeding density.
Unfortunately, sufficient data were not available to investigate the
possibility that breeding synchrony may contribute to low levels of EPP on
islands. The level of breeding synchrony is a potential confounding variable;
however, there is still disagreement over whether it will increase
(Stutchbury and Morton, 1995)
or decrease (Birkhead and Biggins,
1987; Sherman and Morton,
1988) the level of EPP. The idea that there is a simple
relationship between the level of breeding synchrony and the level of EPP has
provoked controversy and has yet to receive any unequivocal empirical support
(see Westneat and Sherman,
1997; Weatherhead and
Yezerinac, 1998). It is difficult to imagine why island
populations may exhibit the sort of consistent significant differences in the
degree of breeding synchrony that would be needed to cause low levels of EPP,
even assuming there is a relationship between synchrony and EPP. Finally, of
the island populations cited in this study, several specifically cast doubt on
the ability of the synchrony hypothesis to explain the low levels of EPP in
their populations. For example, the common occurrence of asynchronous second
and third broods means that the populations have both synchronous and
asynchronously breeding individuals (e.g.,
Griffith et al., 1999;
Petren et al., 1999;
Verboven and Mateman,
1997).
In conclusion, it appears that island populations are characterized by extremely low levels of EPP relative to populations on larger landmasses. This result is consistent with other observations suggesting that the intensity of sexual selection is lower in island populations. Although the cause of this relationship may be at least partly due to the low genetic variation of some island populations, it may also be largely determined by nongenetic factors which require further investigation. That island populations are so different with respect to such an important aspect of behavioral ecology is of great importance from both a conservation view and because island populations are often used as model populations for the study of behavioral and evolutionary ecology.
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ACKNOWLEDGEMENTS |
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Thanks to Terry Burke, Anders Møller, Ian Owens, Marion Petrie, Ben Sheldon, and Dave Westneat for discussion and ideas and two anonymous referees for comments on the manuscript. This work was supported by the UK Natural Environment Research Council and a grant from the Swedish Natural Sciences Research Council to Ben Sheldon.
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