Behavioral Ecology Vol. 12 No. 6: 674-680
© 2001 International Society for Behavioral Ecology
No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus)
a Division of Biological Sciences, Institute of Environmental and Natural Sciences, Lancaster University, Lancaster LA1 4YQ, UK b Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK c Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18D, S 752 36 Uppsala, Sweden
Address correspondence to I.R. Hartley. E-mail: i.hartley{at}lancaster.ac.uk . I.R.K. Stewart is now at the T.H. Morgan School of Biology, University of Kentucky, Lexington, KY 40506-0225, USA. S.C. Griffith is now at the Department of Zoology, Oxford University, South Parks Road, Oxford OX1 3PS, UK.
Received 29 June 2000; revised 5 December 2000; accepted 11 December 2000.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Sex allocation theory predicts that parents should manipulate brood sex ratio in order to maximise the combined reproductive value of their progeny. Females mating with high quality males should, therefore, be expected to produce brood sex ratios biased towards sons, as male offspring would receive a relatively greater advantage from inheritance of their father's characteristics than would their female siblings. Furthermore, it has been suggested that sex allocation in chicks fathered through extrapair fertilizations should also be biased towards sons. Contrary to these predictions, we found no evidence that the distribution of sex ratios in a sample of 1483 chicks from 154 broods of blue tits (Parus caeruleus) deviated significantly from that of a binomial distribution around an even sex ratio. In addition, we found no significant effect on brood sex ratio of the individual quality of either parent as indicated by their biometrics, feather mite loads, time of breeding, or parental survival. This suggests that females in our population were either unable to manipulate offspring sex allocation or did not do so because selection pressures were not strong enough to produce a significant shift away from random sex allocation. The paternity of 986 chicks from 103 broods was determined using DNA microsatellite typing. Extrapair males sired 115 chicks (11.7%) from 41 broods (39.8%). There was no significant effect of paternity (within-pair versus extrapair) on the sex of individual offspring. We suggest that, in addition to the weakness of selection pressures, the possible mechanisms responsible for the allocation of sex may not be sufficiently accurate to control offspring sex at the level of the individual egg.
Key words: Blue tit, DNA microsatellite typing, extrapair paternity, parental quality, Parus caeruleus, sex ratio.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Sex allocation theory (Charnov, 1982
; Trivers and Willard,
1973) suggests that if females were able to predict the relative
reproductive value of sons and daughters, natural selection would favor
individuals possessing the ability to bias reproduction towards the sex with
the higher value. Sex ratio variation in birds was previously thought to be a
consequence of the random nature of chromosomal segregation during meiosis
(Williams, 1979). Recent
studies, however, have provided evidence that brood sex ratio may be skewed in
an adaptive manner in relation to a variety of factors such as secondary
sexual characteristics (Ellegren et al.,
1996; Sheldon et al.,
1999), male survival (Sheldon
et al., 1999; Svensson and
Nilsson, 1996), local resource enhancement and competition
(Komdeur et al., 1997) and
female body condition (Hornfeldt et al.,
2000; Nager et al.,
1999). The mechanism of sex allocation in birds is not fully
understood, however (Krackow,
1995), and there are other studies where an adaptive brood sex
ratio might be expected but has not been found
(Bradbury et al., 1997;
Fiala, 1981;
Hartley et al., 1999;
Radford and Blakey, 2000;
Saino et al., 1999;
Westerdahl et al., 1997).
When the population sex ratio is even, the mean reproductive value of male
and female offspring is equal (Fisher,
1930), but that of individual males and females may vary according
to their different mating opportunities. While the variance in reproductive
success is generally most pronounced in a polygynous mating system, it also
varies in monogamous systems where extrapair fertilizations occur (e.g.,
Kempenaers et al., 1997).
Females only raise a single brood per reproductive attempt, whereas males
possess a higher reproductive potential with a greater variance. A male's
mating success may be determined by the quality of sexually selected traits he
displays (Owens and Hartley,
1998). By assessing the secondary sexual characteristics of the
father(s) of her brood, a female would, in theory, be able to predict the
reproductive value of her offspring and bias the sex ratio accordingly. We
would predict, therefore, that females mated to attractive or successful males
should produce a brood sex ratio skewed towards males, whereas a female mated
to a poor quality male would maximize the reproductive value of her offspring
by producing a female-biased brood
(Burley, 1986;
Burley and Calkins, 1999).
Recent studies have produced conflicting results. Significant positive
correlations have been found between blue tit Parus caeruleus brood
sex ratios (proportion of offspring which were sons) and both male survival
prospects (Svensson and Nilsson,
1996) and the secondary sexual characteristic of plumage
reflectance (Sheldon et al.,
1999). However, no relationship was found between offspring sex
ratio and male mating success in corn buntings Miliaria calandra
(Hartley et al., 1999) or barn
swallows Hirundo rustica (Saino
et al., 1999).
It may be costly for females to engage in extrapair copulations (EPCs;
Birkhead and Møller,
1992) and, therefore, a net benefit would only be gained if the
offspring produced were of a higher reproductive value than those produced by
mating with the pair male. Males engaging in EPCs are therefore predicted to
be of higher relative quality in comparison to a female's social partner
(Otter et al., 1998;
Whittingham and Lifjeld, 1995;
but see Stutchbury et al.,
1997). We would consequently predict a male-biased sex ratio
amongst extrapair chicks. However, no such relationship has been found in the
few recent studies in birds (Saino et al.,
1999; Sheldon and Ellegren,
1996; Westerdahl et al.,
1997), although some preliminary data for blue tits suggests that
extrapair chicks are more likely to be male
(Kempenaers et al., 1997).
The aim of this study is to investigate the effects of parental quality and offspring paternity on brood sex ratios in the blue tit. Parental quality was assessed using biometric measurements and survival to subsequent breeding seasons, while paternity was determined using DNA microsatellite markers.
|
METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Field measurements
Data were collected during the breeding seasons of 1997 to 1999 from box nesting blue tits in six separate, small (< 30 ha) deciduous and mixed woods in northwest Lancashire, U.K. Adult birds were caught at feeding stations during the winter using mist nets or at the nest while provisioning nestlings. The majority of adult birds were individually marked with a numbered metal ring and a combination of three color rings so that they could be identified in the field.
Body size, ectoparasite load, extent of post-juvenal molt and over-winter
survival were identified as potential indicators of individual quality. Body
size may influence the ability to compete for food
(Garnett, 1981) and obtain a
breeding territory (Drent,
1983). Right wing length (maximum chord to nearest mm), right
tarsus length (to nearest 0.1mm) and mass (to nearest 0.1g) were recorded
using a fixed rule, calipers, and a spring balance respectively. Repeatability
(r) values for tarsus and wing length were calculated according to the method
in Lessells and Boag (1987),
and were based on data collected by three observers, with individual birds
measured at approximately annual intervals. Tarsus length was significantly,
moderately repeatable (r =.42, F110, 141 = 2.62,
p <.001) while wing length showed a significant high repeatability
(r =.78, F110, 141 = 8.88, p <.001;
interpretation of r values taken from
Martin and Bateson, 1986).
Parasites may reduce host reproductive success and survival
(Loye and Zuk, 1991) and
therefore influence quality. An ectoparasite load was calculated by scoring
the presence of feather mites mites (Acari: Proctophyllodidae) of the species,
Proctophyllodes stylifer (Buckholz), on each primary, secondary and
tertial feather on a scale of 0-3 (representing zero-light-medium-heavy
infestation). An index of mite infestation was calculated by totaling the
scores for each of the 19 remiges (Behnke
et al., 1999; Wiles et al.,
2000).
Age was assessed using plumage characteristics according to Svensson
(1984). As the extent of
post-juvenal molt may reflect body condition
(Gosler, 1991), post-juvenal
molt was recorded as the number of juvenal greater secondary coverts retained
on the right wing. Molt was scored from 9 (all juvenal coverts retained)
through zero (no juvenal coverts retained but alular, or "bastard
wing," feathers all retained) to -2 (all juvenal coverts and the larger
two feathers on the alular molted and replaced), so that a lower score
indicated that the molt had progressed further before suspension
(Ginn and Melville, 1983).
Molt scores for adult birds (more than 1 year old) are unavailable as all blue
tits undergo a complete plumage molt after breeding and show no variance in
the procedure after their first year.
A measure of over-winter survival was obtained using recapture data or
sightings of color-ringed birds. As the dispersal of breeding blue tits was
very low in this population (unpublished data), all breeding individuals that
were not found in the study area during any subsequent breeding season were
considered to have died (Svensson and
Nilsson, 1996).
Blood samples (20-50µl) were taken from the brachial or tarsal vein under Home Office and English Nature licenses and stored in 100% ethanol. Unhatched eggs were removed from the nest several days after the rest of the clutch had hatched. Dead embryos were removed and stored in 100% ethanol. Tissue samples were taken from any chick found dead prior to blood sampling and stored in 100% ethanol. Nests were visited every 2-3 days to establish the first egg date, clutch size, date at which incubation began, hatching date, hatching success and the number of chicks that fledged.
Molecular methods
Sexing techniques
DNA was made available for amplification either by a standard
proteinase-K/phenol chloroform extraction
(Kawasaki, 1990) or through a
Chelex® resin-based technique (Walsh
et al., 1991). Sex was determined by polymerase chain reaction
(PCR) amplification of the CHD1-W and CHD1-Z genes using the
primers P2 and P8 (Griffiths et al.,
1998). Products amplified from the 1997 and 1998 samples were
separated by electrophoresis through 6% denaturing polyacrylamide gels and
visualized by silver staining (Bassam et
al., 1991). In 1999, products were separated in 2.5% agarose gels
containing ethidium bromide and visualized under UV light. The CHD1-W
gene is on the W chromosome and CHD1-Z on the Z chromosome. In birds,
the heterogametic female possesses both genes, while the male possesses only
CHD1-Z. In blue tits the product amplified from the CHD1-W
gene is 25 base pairs larger than the product for the CHD1-Z gene
and, therefore, a female sample exhibits two clear bands in contrast to the
single band of a male sample. To validate our procedures, PCR products for 172
birds of known gender (from behavioral observations) were blindly scored for
sex. These results agreed with the field sexings in 99.4% (171/172) of cases.
The one disagreement was probably the result of a mistake in the field when
reading rings or in the laboratory with tube labeling.
Paternity analysis
Paternity was analyzed using PCR amplification of 11 polymorphic DNA
microsatellite loci (Table 1).
Novel loci that increased the power of the analysis became available as the
project proceeded and, accordingly, the set used varied between subsets of the
data. Products were separated in 6% polyacrylamide gels and visualized using
silver staining (Bassam et al.,
1991). Allele sizes were calculated by direct comparison between
individuals and by using a 10 base-pair size marker (Life Technologies). The
accuracy of assignment is measured by the exclusion probability of each array,
where exclusion probability is defined as the likelihood of a nestling being
correctly assigned paternity if its genotype matches that of the putative
father at all loci used in the array. All arrays used had a minimum exclusion
probability of 0.976 as calculated by a maximum likelihood procedure using the
CERVUS computer program (Marshall et al.,
1998) (Array A = 0.976, B = 0.985, C = 0.997, D = 0.996;
Table 1). Offspring mismatching
the putative father at any locus were assigned as resulting from extrapair or
within-pair fertilizations according to the maximum likelihood procedure used
in the CERVUS computer program (Marshall
et al., 1998), where the confidence level for assignment was set
at a minimum of 80%. The program calculates the likelihood that a putative
male is the true father given the observed genotypes and their relative
frequency in the population (Marshall et
al., 1998).
|
Statistical methods
Brood sexes are expressed as the proportion of sexed individuals that were
male. Analyses were performed in S-Plus 2000 and follow the methods used by
Westerdahl et al. (1997). For
the main analysis of brood sex ratio and offspring sex, we used generalized
linear models (GLM) with binomial errors and a logit link
(McCullagh and Nelder, 1989;
Venables and Ripley, 1999).
The statistical significance of various terms in the model is determined by
calculating the deviance of the model with and without those terms, where the
deviance is distributed approximately as 
2
(Crawley, 1993). To test the
overall sex ratio distribution for departure from a binomial distribution we
use a robust randomization method which incorporates an element to account for
variable brood sizes (Westerdahl et al.,
1997).
In the analysis of sex ratio in relation to parental characteristics we use
the brood as the unit of analysis and the number of chicks sexed as the
binomial denominator. In the analysis of offspring sex in relation to
paternity we use the chick as the unit of analysis but enter a term as a
nest-box identifier into the model to control for any effects of shared
origin. Additionally, we allowed for any over-dispersion that this may cause
by setting the dispersion parameter according to the variance of the data
(McCullagh and Nelder, 1989)
although in practice, for both models, the dispersion parameter was
approximately one, as expected for binomial data. Power analysis was carried
out for nonsignificant (ns) results and follows the procedures in Cohen
(1976) and the
G*Power computer program (Faul
and Erdfelder, 1992).
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Brood sex ratio and parental quality
During the three study years, the sexes of 1483 chicks from 154 broods were determined, of which 712 were male. The mean brood sex ratio was 0.48 (range = 0.00-0.88, SD = 0.16) (Figure 1). The number of sons and daughters from each brood did not differ significantly (paired t test, t = 1.83, df = 153, p =.069), although there was a tendency for a skew towards daughters. The power of these t tests was relatively high (Power = 92% for a medium to small effect size of d = 0.4). We were unable to sex 146 individuals (9.0% of the total number of eggs laid) due to either eggs being infertile (N = 72), early hatchling mortality, or failure to obtain PCR products, and, therefore, the values given above may differ from those for the primary sex ratio. There was no significant difference between the mean sex ratio of completely and incompletely sexed broods (two sample t test, t = 0.26, df = 152, p =.98). This does not, however, necessarily suggest that our sex ratio values reflected the primary sex ratio before any differential mortality of sons and daughters had occurred prior to sample collection (Fiala, 1981
).
|
The distribution of brood sex ratios did not differ significantly from a
binomial distribution (n = 154, p =.90, 65% power of
detecting a skew as small as 0.60 sons to 0.40 daughters). A similar result
was found even if unsexed offspring were presumed to be either all male or all
female and sex ratios were recalculated accordingly (maximum male skew,
p =.12; maximum female skew, p =.10). This result suggests
that the female blue tits in our study did not manipulate brood sex ratio away
from a random allocation between the sexes, although it does not exclude the
possibility. A repeatability analysis
(Lessells and Boag, 1987)
showed no significant repeatability in brood sex ratio between years for males
(n = 29, r = 0.17, F28, 36 = 1.46, p
=.14) or for females (n = 19, r = -.20, F18,
21 = 0.65, p =.82). The lack of repeatability indicates that
any variation in brood sex ratio was not due to consistent individual
differences between breeding birds, and so we are justified in using each
breeding attempt as the unit of analysis in our following tests. Unfortunately
the power of these two tests is low (16-20% for a large effect size of
f2 = 0.35). We therefore repeated all our analyses using a
reduced data set to which all breeders contributed only once. The reduced data
set contained about 12% fewer breeding attempts but the results did not differ
from the main analysis. The results for the full data set are reported
here.
The results of the generalized linear model (Table 2) show that there were no significant effects on brood sex ratio of male or female biometrics or survival, year, breeding wood, date of breeding, clutch size or fledging success (number of chicks fledged). The GLM in Table 2 was repeated for first year males and females separately to include a variable that scores the extent of post-juvenal molt. The model remained qualitatively the same and the extent of post-juvenal molt in breeding birds did not influence their brood sex ratio (male molt, change in deviance = 0.0001, df = 1, ns; female molt, change in deviance = 1.54, df = 1, ns). The statistical power of each GLM is given in the tables.
|
Offspring sex and paternity
We could check the putative parentage of 986 chicks from 103 broods. Using
CERVUS (Marshall et al., 1998;
Slate et al., 2000), we could
exclude the putative father as the most likely genetic father for 115
offspring (11.7% of chicks from 41 [39.8%] broods) and this exclusion
likelihood was statistically significant for 89 of these offspring. Here, we
treat all 115 offspring as being the result of extrapair fertilizations. If we
only treat as extrapair those 89 offspring for which paternity was
significantly more likely to be due to a nonputative father, the conclusions
of the following analysis remain the same. We were unable to determine
paternity for a further 49 offspring/eggs from these broods (4.97% of the
total number of offspring) due to mortality prior to sampling or failure to
obtain PCR products. The distribution of extrapair chicks among broods was
significantly different from a binomial distribution (calculated as above and
Westerdahl, 1997 n =
95, p <.0001). If we conservatively take the two extreme cases, in
which all chicks for which paternity had not been determined were assigned
either as within-pair, or as extrapair, and the test was repeated in each
case, the result remained the same. A repeatability analysis for extrapair
fertilizations containing both completely within-pair and mixed paternity
broods showed a significant, moderate repeatability for individual males
between years (n = 12, r =.59, F10, 12 =
4.79, p =.006), suggesting that some individuals are consistently
susceptible to cuckoldry regardless of their age. A similar test could not be
performed for females due to the small sample size.
A comparison of extrapair offspring frequency with sex ratio across broods,
as suggested by Westneat et al.
(1995), provides one test for
a positive correlation between sex ratio and level of extrapair paternity.
However, as noted by Sheldon and Ellegren
(1996), if females mated to
high quality males are biasing their brood sex ratio towards sons whilst not
actively pursuing extrapair copulations, a negative correlation is predicted.
The effect of paternity on offspring sex was therefore analyzed at the level
of the individual chick using a GLM, controlling for the effects of common
brood (see Statistical Methods section). The results show that neither the
paternity of the chick (within-pair or extrapair father) nor the paternity of
the brood (mixed paternity or single father) had any significant effect on the
sex of offspring (Table 3),
which implies that female blue tits in our study were not assigning individual
chicks to a particular sex on the basis of paternity.
|
The significant effect of the interaction between brood and paternity indicates that the size of the difference between within-pair and extrapair sex ratios varies significantly between some broods. To investigate this further, we calculated the sex ratio difference for each brood (within-pair chicks' sex ratio minus extrapair chicks' sex ratio), and compared this between years and breeding woods. There was no significant effect of year or wood on sex ratio difference, although there was a trend towards an effect of breeding wood (two-way ANOVA, Year F1,33 = 0.07, p =.79; Wood F3,33 = 2.86, p =.052; Year x Wood interaction, F3,33 = 0.28, p =.84). We could find no other consistent effects to explain the significant interaction between brood and paternity.
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Male quality and brood sex ratio
The distribution of brood sex ratios in our study population was not significantly different from binomial with a sample size which was large relative to that of previous studies of blue tits (1483 chicks from 154 broods in comparison with 389 chicks from 41 broods [Svensson and Nilsson, 1996
]
and 590 chicks from 57 broods [Sheldon et
al., 1999]). We found no significant effects on brood sex ratio of
our measures of parental quality, brood size or brood fledging success.
Neither were there consistent differences in brood sex ratio between the three
years of our study, nor between our study sites.
While many studies of passerine birds have found no evidence for consistent
brood sex ratio skews (e.g., Bradbury et
al., 1997; Fiala,
1981; Koenig and Dickinson,
1996; Lombardo,
1982; Patterson and Emlen,
1980; Saino et al.,
1999; Westneat et al.,
1995), others have found very different and potentially exciting
results. A number of recent studies on Parus species have
demonstrated significant correlations between brood sex ratio and various
indicators of male quality, including body size
(Kolliker et al., 1999),
over-winter survival (Svensson and
Nilsson, 1996) and plumage characteristics
(Sheldon et al., 1999). In all
cases, females paired with supposedly higher quality males tended to produce
offspring sex ratios that were skewed towards males, which suggests that
females are able to bias sex ratio towards the sex with the higher
reproductive value.
If it is assumed that all females assess male quality in a similar manner,
a consistent response to a given male in successive years would be predicted
if brood sex ratio had been manipulated in an adaptive manner. In our study,
however, the brood sex ratio for individual males was not consistent between
years (Lessells and Quinn,
1999). The relationship between male age and sex ratio was also
not significant, indicating that this result was not due to the change, over
time, of cues reflecting male quality.
Brood sex ratio did not show a significant relationship with any of the
biometrics measured as indicators of male quality, nor did we find a
significant effect of male parasite load, although we did not measure the UV
reflectance of the crown feathers which is a recently discovered secondary
sexual characteristic (Andersson et al.,
1998; Hunt et al.,
1998; Sheldon et al.,
1999). In contrast with previous findings
(Svensson and Nilsson, 1996)
and with a larger sample size, we found no relationship between male
over-winter survival and the brood sex ratio produced during the previous
breeding season.
One interpretation of our results is that females were unable to assert any
control over the sex ratio of their offspring, but data from other studies
suggests that this is not always the case
(Komdeur et al., 1997;
Sheldon et al., 1999). The
mechanisms which enable the adaptive manipulation of brood sex ratio may be
constrained by the differential costs of producing male and female offspring.
This may be of greater consequence in birds where a marked size dimorphism
generally exists between the sexes at a very early stage of development
(Rosenfield et al., 1996) but
may have an effect in blue tits as male chicks are generally heavier than
females (Hartley IR, Stewart IRK, Royle NJ, in preparation).
It is difficult to account for the apparent differences between populations
of the same species, both within this study and between studies, because few
data are available, although the variance in the intensity of selection
pressures between populations may be an important factor
(Dale et al., 1999;
Griffith et al., 1999). A
female-biased operational sex ratio would result in decreased selection
pressure on traits used by females to determine male quality, reducing the
reliability of the signal and thus a female's ability to assess male status
and adjust the brood sex ratio accordingly. However, the nonrandom occurrence
of extrapair fertilizations in our population suggests that variation in
female assessment of male quality should occur. Variability of environmental
selection pressures could also explain the between-population variance in
correlates of sex ratio. An alternative hypothesis suggests that females
adjust brood sex ratio in relation to territory quality
(Richner et al., 1993) which
may be positively correlated with male quality. We have no measure of
territory quality in our study, but if it shows little variance then the
selection pressure for adaptive sex ratio manipulation might be low. We found
no significant effect of fledging success, independently of clutch size, on
brood sex ratio, indirectly suggesting that territory quality, or factors that
influence nest productivity did not influence the brood sex ratio.
Female quality and brood sex ratio
The maternal condition hypothesis
(Trivers and Willard, 1973)
predicts that females should adjust their brood sex ratio according to their
own condition when eggs are laid, although male quality may be a confounding
variable in populations where assortative mating occurs, as in the blue tit
(Andersson et al., 1998). A
study on lesser black-backed gulls, Larus fuscus, provides
experimental evidence supporting this theory; females in better body condition
tended to have more sons (Nager et al.,
1999). However, we found no significant relationship between any
of our measures of female quality and brood sex ratio, a similar result to
that found in several other observational studies on passerines (e.g.,
Bradbury et al., 1997;
Kolliker et al., 1999;
Westerdahl et al., 1997; but
see Westerdahl et al., 2000).
These results indicate either that our measures do not provide an accurate
indication of female condition, or that variation in female quality is not
sufficient to instigate a detectable level of variance among sex ratios
between broods in our population.
Paternity and brood sex ratio
The distribution of extrapair paternity among broods in our population
differed significantly from that expected due to random allocation, suggesting
that there was significant variation in the probability of a male's nest
containing chicks fathered through extrapair copulation. There was, however,
no significant relationship between the sex of a chick and its paternity,
which might be expected if females were able to manipulate the sex allocation
adaptively to individual chicks. This result matches the findings of most
previous studies, both observational
(Sheldon and Ellegren, 1996;
Westerdahl et al., 1997) and
experimental (Saino et al.,
1999), although it differs from the preliminary results found in
another study of blue tits, where there was a suggestion that extrapair
offspring were more likely to be male
(Kempenaers et al., 1997).
We may not have measured the trait that is important in determining the incidence of extrapair paternity in our population. Preliminary analysis suggests that the proportion of extrapair nestlings in a brood is unrelated to the male nest holder's biometrics or breeding age, although there was a significant effect with the wood in which the birds bred, suggesting that habitat features may be important in determining the incidence of extrapair paternity (unpublished data). Despite this, there was no effect of the breeding wood on sex ratio in the above analyses.
Although we found no evidence for selection on sex allocation, the
mechanisms of the procedure may not be accurate enough to target specific
eggs. Sheldon and Ellegren
(1996) proposed that either
females might be able to "identify" the sperm of a particular male
and allocate it to a specific egg, or that the probability of each egg
producing a particular sex may vary according to its position in the laying
sequence. This could possibly be caused by variation in hormone levels during
the laying period (Gil et al.,
1999, but see Birkhead et al.,
2000).
Several studies have identified a significant relationship between chick
sex and laying order, offering support for the second hypothesis
(Ankney, 1982;
Dijkstra et al., 1990),
although other similar studies have failed to find an effect
(Cooke and Harmsen, 1983;
Leblanc, 1987). The successful
pursuit of extrapair copulations by either sex may vary in feasibility over
time due to constraints such as mate guarding by either sex
(Baltz and Clark, 1997) or
local competition. The possibility of achieving a successful extrapair
copulation at the right time may therefore be too unpredictable to allow the
female to specify the sex of each egg independently. In addition, the low
level of predictability concerning the outcome of fertilizations
(Colegrave et al., 1995) may
hamper the specificity of this mechanism.
|
ACKNOWLEDGEMENTS |
|---|
We would like to thank Richard du Feu and Phil Smith for help with fieldwork, Kate Lessells for useful discussions and comments on the manuscript, Ken Wilson and Ian Hardy for advice about statistical analysis, Stephen Tanner and David Richardson for the use of their unpublished primers, and Andy Krupa, Deborah Dawson, and Mark Wilson at the NERC-funded Sheffield Molecular Genetics Facility for assistance with the DNA analysis. The work was funded by a NERC studentship to David Leech, the Royal Society and the British Ecological Society.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson S, Ornborg J, Andersson M, 1998. Ultraviolet sexual dimorphism and assortative mating in blue tits. Proc R Soc Lond B 265: 445-450.
Ankney CD, 1982. Sex ratio varies with egg sequence in Lesser Snow Geese. Auk 99: 662-666.
Baltz AP, Clark AB, 1997. Extra-pair courtship behaviour of male budgerigars and the effect of an audience. Anim Behav 53: 1017-1024.
Bassam BJ, Caetanoanolles G, Greshoff PM, 1991. Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 196: 80-83.[ISI][Medline]
Behnke J, McGregor P, Cameron J, Hartley I, Shepherd M, Gilbert F, Barnard C, Hurst J, Gray S, Wiles R, 1999. Semi-quantitative assessment of wing feather mite (Acarina) infestations on passerine birds from Portugal—Evaluation of the criteria for accurate quantification of mite burdens. J Zool 248: 337-347.
Bensch S, Price T, Kohn J, 1997. Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol Ecol 6: 91-92.[Medline]
Birkhead TR, Møller AP, 1992. Sperm competition in birds: evolutionary causes and consequences. London: Academic Press.
Birkhead T, Schwabl H, Burke T, 2000. Testosterone and maternal effects—integrating mechanisms and function. Trends Ecol Evol 15: 86-87.[Medline]
Bradbury RB, Cotton PA, Wright J, Griffiths R, 1997. Nestling sex ratio in the European starling (Sturnus vulgaris). J Avian Biol 28: 255-258.
Burley N, 1986. Sex-ratio manipulation in color-banded populations of zebra finches. Evolution 40: 1191-1206.
Burley NT, Calkins JD, 1999. Sex ratios and sexual
selection in socially monogamous zebra finches. Behav Ecol
10: 626-635.
Charnov EL, 1982. The theory of sex allocation. Princeton, New Jersey: Princeton University Press.
Cohen J, 1976. Statistical power analysis for the behavioral sciences. London: Academic Press.
Colegrave N, Birkhead TR, Lessells CM, 1995. Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proc R Soc Lond B 259: 223-228.
Cooke F, Harmsen R, 1983. Does sex ratio vary with egg sequence in Lesser Snow Geese? Auk 100: 215-217.
Crawley MJ, 1993. GLIM for ecologists. Oxford: Blackwell Scientific.
Dale S, Slagsvold T, Lampe HM, Saetre GP, 1999. Population divergence in sexual ornaments: the white forehead patch of Norwegian pied flycatchers is small and unsexy. Evolution 53: 1235-1246.
Dawson DA, Hanotte O, Greig C, Stewart IRK, Burke T, 2000. Polymorphic microsatellites in the blue tit Parus caeruleus and their cross-species utility in twenty songbird families. Mol Ecol 9: 1941-1944.[Medline]
Dijkstra C, Daan S, Buker JB, 1990. Adaptive seasonal variation in the sex ratio of kestrel broods. Funct Ecol 4: 143-147.
Double MC, Cockburn A, 2000. Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc R Soc Lond B 267: 465-470.[Medline]
Double MC, Dawson D, Burke T, Cockburn A, 1997. Finding the fathers in the least faithful bird: A microsatellite-based genotyping system for the superb fairy-wren Malurus cyaneus. Mol Ecol 6: 691-693.
Drent PJ, 1983. The functional ethology of territoriality in the great tit (Parus major L.) (PhD dissertation). Groningen: Groningen University.
Ellegren H, Gustafsson L, Sheldon BC, 1996. Sex ratio
adjustment in relation to paternal attractiveness in a wild bird population.
Proc Natl Acad Sci 93:
11723-11728.
Faul F, Erdfelder E, 1992. G*Power: A-priori, post-hoc and compromise power analysis for MS-DOS [computer program]. Bonn University.
Fiala KL, 1981. Sex ratio constancy in the red-winged blackbird. Evolution 35: 898-910.
Fisher RA, 1930. Genetical theory of natural selection. London: Clarendon Press.
Garnett MC, 1981. Body size, its heritability and influence on juvenile survival among great tits, Parus major. Ibis 123: 31-41.
Gil D, Graves J, Hazon N, Wells A, 1999. Male
attractiveness and differential testosterone investment in zebra finch eggs.
Science 286:
126-128.
Ginn H, Melville D, 1983. Moult in birds. Tring, UK: British Trust for Ornithology.
Gosler AG, 1991. On the use of greater covert moult and pectoral muscle as measures of condition in passerines with data for the Great Tit Parus major. Bird Stud 38: 1-9.
Griffith SC, Owens IPF, Burke T, 1999. Female choice and annual reproductive success favour less-ornamented male house sparrows. Proc R Soc Lond B 266: 765-770.
Griffiths R, Double MC, Orr K, Dawson RJG, 1998. A DNA test to sex most birds. Mol Ecol 7: 1071-1075.[Medline]
Hartley IR, Griffith SC, Wilson K, Shepherd M, Burke T, 1999. Nestling sex ratios in the polygynously breeding corn bunting Miliaria calandra. J Avian Biol 30: 7-14.
Hornfeldt B, Hipkiss T, Fridolfsson AK, Eklund U, Ellegren H, 2000. Sex ratio and fledging success of supplementary-fed Tengmalm's owl broods. Mol Ecol 9: 187-192.[Medline]
Hunt S, Bennett ATD, Cuthill IC, Griffiths R, 1998. Blue tits are ultraviolet tits. Proc R Soc Lond B 265: 451-455.
Kawasaki ES, 1990. Sample preparation from blood, cells, and other fluids. In: PCR protocols: a guide to methods and applications (Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds). London: Academic Press; 146-152.
Kempenaers B, Verheyen GR, Dhondt AA, 1997. Extrapair
paternity in the blue tit (Parus caeruleus): female choice, male
characteristics and offspring quality. Behav Ecol
8: 481-492.
Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broeckhoven C, Dhondt AA, 1992. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357: 494-497.
Koenig WD, Dickinson JL, 1996. Nestling sex ratio variation in western bluebirds. Auk 113: 902-910.
Kolliker M, Heeb P, Werner I, Mateman AC, Lessells CM, Richner H,
1999. Offspring sex ratio is related to male body size in the
great tit (Parus major). Behav Ecol
10: 68-72.
Komdeur J, Daan S, Tinbergen J, Mateman C, 1997. Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature 385: 522-525.
Krackow S, 1995. Potential mechanisms for sex ratio adjustment in mammals and birds. Biol Rev 70: 225-241.[Medline]
Leblanc Y, 1987. Egg mass, position in the laying sequence, and brood size in relation to Canada Goose reproductive success. Wilson Bull 99: 663-672.
Lessells CM, Boag PT, 1987. Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.[ISI]
Lessells CM, Quinn JS, 1999. Primary sex ratios: Variation, causes and consequences. In: Proceedings 22nd International Ornithological Congress, 16-22 August 1998, Durban; 27.
Lombardo MP, 1982. Sex ratios in the eastern bluebird. Evolution 36: 615-617.
Loye JE, Zuk M (Eds), 1991. Bird-parasite interactions: ecology, evolution and behaviour. Oxford: Oxford University Press.
Marshall TC, Slate J, Kruuk L, Pemberton JM, 1998. Statistical confidence for liklihood-based paternity inference in natural populations. Mol Ecol 7: 639-655.[Medline]
Martin P, Bateson P, 1986. Measuring behaviour: an introductory guide. Cambridge: Cambridge University Press.
McCullagh P, Nelder JA, 1989. Generalized linear models. London: Chapman and Hall.
Nager RG, Monaghan P, Griffiths R, Houston DC, Dawson R,
1999. Experimental demonstration that offspring sex ratio varies
with maternal condition. Proc Natl Acad Sci
96: 570-573.
Otter K, Ratcliffe L, Michaud D, Boag PT, 1998. Do female blackcapped chickadees prefer high-ranking males as extra-pair partners? Behav Ecol Sociobiol 43: 25-36.
Owens IPF, Hartley IR, 1998. Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B 265: 397-407.
Patterson CB, Emlen JM, 1980. Variation in nestling sex-ratios in the yellow-headed blackbird. Am Nat 115: 743-747.
Radford AN, Blakey JK, 2000. Is variation in brood sex
ratios adaptive in the great tit (Parus major)? Behav
Ecol 11:
294-298.
Richardson D, Jury F, Dawson D, Salguiero P, Komdeur J, Burke T, 2000. Fifty Seychelles warbler (Acrocephalus sechellensis) microsatellite loci polymorphic in Sylviidae species and their cross-species amplification in other passerine birds. Mol Ecol 9: 2226-2231.[Medline]
Richner H, Oppliger A, Christe P, 1993. Effect of an ectoparasite on reproduction in great tits. J Anim Ecol 62: 703-710.
Rosenfield RN, Bielefeldt J, Vos SM, 1996. Skewed sex ratios in Cooper's hawk offspring. Auk 113: 957-960.
Saino N, Ellegren H, Møller AP, 1999. No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows. Mol Ecol 8: 399-406.
Sheldon BC, Andersson S, Griffith SC, Ornborg J, Sendecka J, 1999. Ultraviolet colour variation influences blue tit sex ratios. Nature 402: 874-877.
Sheldon BC, Ellegren H, 1996. Offspring sex and paternity in the collared flycatcher. Proc R Soc Lond B 263: 1017-1021.
Slate J, Marshall T, Pemberton J, 2000. A retrospective assessment of the accuracy of the paternity inference program CERVUS. Mol Ecol 9: 801-808.[Medline]
Stutchbury BJM, Piper WH, Neudorf DL, Tarof SA, Rhymer JM, Fuller G, Fleischer RC, 1997. Correlates of extra-pair fertilisation success in hooded warblers. Behav Ecol Sociobiol 40: 119-126.
Svensson E, Nilsson J, 1996. Mate quality affects offspring sex ratio in blue tits. Proc R Soc Lond B 263: 357-361.
Svensson L, 1984. Identification guide to European passerines, 3rd ed. Stockholm: British Trust for Ornithology.
Trivers RL, Willard DE, 1973. Natural selection of
parental ability to vary the sex ratio of offspring. Science
179: 90-92.
Valdes AM, Slatkin M, Freimer NB, 1993. Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133: 737-749.[Abstract]
Venables WN, Ripley BD, 1999. Modern applied statistics with S-Plus. New York: Springer.
Walsh PS, Metzger DA, Higuchi R, 1991. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506-513.[ISI][Medline]
Westerdahl H, Bensch S, Hansson B, Hasselquist D, Von Schantz T, 1997. Sex ratio variation among broods of great reed warblers Acrocephalus arundinaceus. Mol Ecol 6: 543-548.
Westerdahl H, Bensch S, Hansson B, Hasselquist D, Von Schantz T, 2000. Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus). Behav Ecol Sociobiol 47: 312-318.
Westneat DF, Clark AB, Rambo KC, 1995. Within-brood patterns of paternity and parental behavior in red-winged blackbirds. Behav Ecol Sociobiol 37: 349-356.
Whittingham LA, Lifjeld JT, 1995. Extra-pair fertilizations increase the opportunity for sexual selection in the monogamous house martin Delichon urbica. J Avian Biol 26: 283-288.
Wiles R, Cameron J, Behnke JM, Hartley IR, Gilbert FS, McGregor PK, 2000. Wing feather mite infestations on passerine birds: Season and ambient air temperature influence the distribution of Proctophyllodes stylifer across the wings of blue tits (Parus caeruleus). Can J Zool 78: 1397-1407.
Williams GC, 1979. The question of adaptive sex ratio in outcrossed vertebrates. Proc R Soc Lond B 205: 567-580.[Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  K. E. Delmore, O. Kleven, T. Laskemoen, S. A. Crowe, J. T. Lifjeld, and R. J. Robertson Sex allocation and parental quality in tree swallows Behav. Ecol., August 4, 2008; (2008) arn081v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Dickens and I. R. Hartley Differences in parental food allocation rules: evidence for sexual conflict in the blue tit? Behav. Ecol., July 1, 2007; 18(4): 674 - 679. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Korsten, C. M. Lessells, A. C. Mateman, M. van der Velde, and J. Komdeur Primary sex ratio adjustment to experimentally reduced male UV attractiveness in blue tits Behav. Ecol., July 1, 2006; 17(4): 539 - 546. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Dreiss, M. Richard, F. Moyen, J. White, A.P. Moller, and E. Danchin Sex ratio and male sexual characters in a population of blue tits, Parus caeruleus Behav. Ecol., January 1, 2006; 17(1): 13 - 19. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. E. Johannessen, T. Slagsvold, B. T. Hansen, and J. T. Lifjeld Manipulation of male quality in wild tits: effects on paternity loss Behav. Ecol., July 1, 2005; 16(4): 747 - 754. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A.N. Rutstein, H.E. Gorman, K.E. Arnold, L. Gilbert, K.J. Orr, A. Adam, R. Nager, and J.A. Graves Sex allocation in response to paternal attractiveness in the zebra finch Behav. Ecol., July 1, 2005; 16(4): 763 - 769. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. E. Budden and S. R. Beissinger Against the odds? Nestling sex ratio variation in green-rumped parrotlets Behav. Ecol., July 1, 2004; 15(4): 607 - 613. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Z. Garamszegi and A. P. Moller Extrapair paternity and the evolution of bird song Behav. Ecol., May 1, 2004; 15(3): 508 - 519. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Spottiswoode and A. P. Moller Extrapair paternity, migration, and breeding synchrony in birds Behav. Ecol., January 1, 2004; 15(1): 41 - 57. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. R. Oddie and C. Reim Egg sex ratio and paternal traits: using within-individual comparisons Behav. Ecol., July 1, 2002; 13(4): 503 - 510. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||