OIKOS 109: 367 /373, 2005
Sex ratio of Parus major and P. caeruleus broods depends on parental
condition and habitat quality
Michael Stauss, Gernot Segelbacher, Jürgen Tomiuk and Lutz Bachmann
Stauss, M., Segelbacher, G., Tomiuk, J. and Bachmann, L. 2005. Sex ratio of Parus
major and P. caeruleus broods depends on parental condition and habitat quality.
/ Oikos 109: 367 /373.
Brood sex ratio was studied in 88 families of Parus caeruleus (blue tit) and 95 families
of P. major (great tit) in deciduous and mixed forest habitats differing in food
availability. As a food specialist, the blue tit is expected to be more sensitive to the
nutritional differences between the habitats than a food generalist such as the great tit.
A shift of brood sex ratio towards males was detected for great tits in the high quality
habitat, but there was no significant impact of parental condition or the number of
nestlings. In contrast, brood sex ratio of blue tits was not affected by habitat quality.
In blue tits, male condition correlated positively with a male-biased sex ratio. Habitat
quality, however, affected the body mass differences of male and female blue tit
siblings, and nestlings developed differently. The low quality habitat had a negative
effect on the sexual dimorphism of siblings in male-biased broods, and the condition of
offspring was bad. Nevertheless, sexual dimorphism cannot explain the differences
between great and blue tits with respect to the correlation of sex ratio and individual
condition.
M. Stauss and J. Tomiuk, Section of General Human Genetics, Inst. of Anthropology and
Human Genetics, Univ. of Tübingen, Wilhelmstrasse 27, DE-72074 Tübingen, Germany.
/ G. Segelbacher, Max Planck Research Centre for Ornithology, Vogelwarte Radolfzell,
Schloss Möggingen, Schlossallee 2, DE-78315 Radolfzell, Germany. / L. Bachmann,
Dept of Zoology, Natural History Museums, Univ. of Oslo, PO Box 1172 Blindern, NO0318 Oslo, Norway (bachmann@nhm.uio.no).
Sex ratio theory intends to explain the frequently
observed variation in the proportion of male and female
offspring in natural populations. According to theoretical considerations, sex allocation in offspring is efficient if males compete for good resources, and selection
operates on mate choice. In these cases, females may
invest in the sex that has the highest probability for
survival and future reproductive success. If females are
able to predict the relative reproductive value of their
offspring, those mating with high quality males are
expected to skew the brood sex ratio towards sons.
Accordingly, females in good condition would increase
their fitness by producing sons of high quality, while
females in poor condition would enhance their fitness
by producing daughters rather than sons of poor
quality (Trivers and Willard 1973, Charnov 1982, Trivers
1985).
Chromosomal sex determination (CSD) is expected to
hamper the facultative adjustment of sex ratios (Maynard Smith 1978, Williams 1979, Charnov 1982). However, recent studies on various taxa with CSD have
reported striking shifts in offspring sex ratios that are in
line with the assumption of selection (Wiebe and
Bortolotti 1992, Korpimäki et al. 2000, Whittingham
and Dunn 2000, Whittingham et al. 2002). These studies
indicate that the sex ratio is not completely constrained
by CSD. However, the data are not consistent. Thus,
whether the observed shifts might just represent sample-
Accepted 1 November 2004
Copyright # OIKOS 2005
ISSN 0030-1299
OIKOS 109:2 (2005)
367
size dependent noise around the expected binomial
distribution is in discussion (Williams 1979, Palmer
2000, Krackow 2002).
West and Sheldon (2002) described two situations with
a definite theoretical prediction as to the direction of sex
ratio adjustment. In addition, they showed that birds can
also adjust the offspring sex ratio in the predicted
direction.
i)
ii)
Females produce more sons when mated to
an attractive male because sons have an increased fitness inherited from their high-quality
father.
In cooperatively breeding species, where one sex
helps more than the other, adjusted to the respective environmental conditions offspring sex ratio
is biased toward the sex that provides more
reproductive help. This, however, is not the
case for Parus species and will not be considered
further.
The following hypotheses will be tested:
i)
ii)
Habitat quality and/or the body condition of
parents affect the sex ratio in broods of blue and
great tits. Thus, male-biased sex ratios are expected
in high habitat quality and when parental conditions are good. For example, females in good
condition are more likely to produce male offspring
than females in poor condition.
The low quality habitat differently affects the body
conditions of sons and daughters. Thus, male
development is more negatively affected by bad
environmental conditions than that of females.
Also, such differences are more pronounced in
broods of specialised blue tits than in broods of
the generalist P. major.
Material and methods
Selection of facultative sex ratio variation is only
expected when the increase in fitness due to this
behaviour exceeds the costs. Accordingly, the most
extreme and precise sex ratio variation will be seen in
species where the fitness benefits of facultative sex ratio
adjustment are high and the costs low (West and
Sheldon 2002).
Unfortunately, very little is known about the way in
which selection acts on sex ratio variation in natural
populations. Complex life histories can influence sex
allocation in many ways, and selection for a particular
form of sex allocation behaviour might be obscured.
Furthermore, if selection varies over time and/or between genetically connected populations, it is unlikely
that populations can reach local optima with respect to
sex allocation. Thus, estimating sex ratios of total
populations can provide highly unreliable information
about sex allocation. Patterns of sex ratios can even be
inconsistent across species (West and Sheldon 2002). Our
approach to these problems is to analyse sex ratio
in broods of blue tits (Parus caeruleus ) and great tits
(P. major ) from two habitat types that differ in resource
quality. The high quality habitat is located in deciduous
forests and the low quality habitat is dominated
by coniferous trees. Availability of food is the major
criterion for classifying the habitats since the abundance
of caterpillars, which is the bulk of nestling food, is
on average 50 times higher in deciduous trees than in
coniferous trees (van Balen 1973).
As a food specialist, the blue tit is expected to
be strongly affected by the nutritional differences
between the habitats. As a food generalist, the great
tit (Gibb and Betts 1963, Cowie and Hinsley 1987,
1988) should be affected much less by the differing
habitats.
368
The breeding performance of great and blue tits (Parus
major and P. caeruleus ) was studied in three study plots
near Tübingen, southwest Germany (48833?N, 9800?E).
Two plots (high quality habitat) are /1 km apart and
consist of woodland (9 ha and 16 ha, respectively; with
90% deciduous trees (mainly beeches and oaks: Fagus
sylvatica (67%), oaks Quercus robur (21%) and some
other deciduous trees (3%) and a small number of
coniferous trees as pines Pinus sylvestris and larchs
Larix decidua (9%)). The third study area (low quality
habitat) is a 35 ha forest dominated by 60% coniferous
trees (scots pines and spruces, for more detailed information see Stauss 2000, Stauss et al. 2005).
In total, 95 great tit and 88 blue tit families were
studied comprising of 665 and 670 sexed offspring,
respectively, during the breeding seasons in 1999 and
2000. Nests were checked regularly during the breeding
seasons of 1999 and 2000. First laying date, clutch size,
number of hatched young and fledglings were recorded.
Nestlings and parents were weighed (to the nearest 0.1 g
using a Sartorius balance) and tarsus lengths (to the
nearest 0.1 mm using calipers) were measured 14 /16
days after hatching. Parents were aged and sexed
according to Svensson (1992). All birds were banded
with a numbered aluminium ring.
Blood samples ( /50 ml) were obtained through
tapping the Vena ulnaris and subsequently stored in
250 ml EDTA-buffer in plastic vials to be frozen until
further processing. DNA was isolated using the DNA
Blood Mini Kit (Qiagen). The gender of the offspring
was determined by PCR (Griffiths et al. 1996, 1998). The
primers P8 (5?-CTCCCAAGGATGAGRAAYTG-3?)
and P2 (5?-TCTGCATCGCTAAATCCTTT-3?) were
used to amplify a sex-specific region of the CHD-1
gene on sex chromosomes (Griffiths et al. 1998).
OIKOS 109:2 (2005)
Statistical methods
Two measurements of individual condition were calculated:
i)
ii)
The overall condition was estimated as the ratio of
body mass and tarsus length.
Residuals were determined from the regression
between tarsus length (independent variable) and
body mass (dependent variable) per year across
habitats.
However, no differences were observed when using
overall condition instead of residuals in the subsequent
analysis. Therefore, only data based on overall condition
will be shown.
Mean values of nestling mass, tarsus length and
condition for each sex in each brood were used in order
to avoid pseudoreplication. Data were standardised for
each year across habitats using z-transformation with
mean/0 and variance /1 in order to eliminate year
effects (for all parameters except residuals).
When brood sex ratio is considered as a dependent
variable, generalised linear models with the number of
sons were used as response variable, and the number of
sexed nestlings were used as binomial denominator
(procedure genmod, SAS 1997). These models are
binomial, and the option link /logit and type 3 for the
likelihood ratio statistics w was used. The effects that
habitat type and sex ratio has on the development of
broods (differences in body traits between male and
female offspring) were tested using a generalised linear
model (procedure glm with type III, SAS 1997).
mentioned parameters and were thus excluded from
further analyses.
Great tit
i)
ii)
iii)
The analyses revealed a significant impact of
habitat quality on brood sex ratio (p /0.03,
Table 1) with a male-bias in the high quality
habitat. In contrast, no statistically significant
impact of the number of nestlings (p /0.64,
Table 1) and the parental condition (p /0.08,
Table 1) on brood sex ratio could be detected.
Brood sex ratio and habitat quality together have
a significant impact on the development of siblings.
This is depicted by the significance of the statistical
model (p /0.03, Table 2). In contrast, habitat
quality, sex ratio and sex ratio nested within habitat
individually have no significant effect on the
development of siblings (0.053B/pB/0.107, Table
2).
Depending on the brood sex ratio, sexual dimorphism in siblings develops differently in both habitats
(Fig. 1a). Differences in body mass between male
and female siblings increases more in male-biased
broods in the high quality habitat (p /0.01) than in
the low quality habitat. In the low quality habitat,
brood sex ratio does not affect sexual dimorphism
in broods (p/0.95).
Blue tit
Results
In total, 95 great tit and 88 blue tit families were studied
comprising of 665 and 670 sexed offspring, respectively.
There was no significant deviation from the expected
50:50 sex ratio of offspring across broods in both
habitats (testing for binomial distribution, p /0.05; great
tit (male/male/female): 0.549/0.02 (se) in deciduous
forest, 0.509/0.03 in coniferous forest; blue tit: 0.499/
0.04 in deciduous forest, 0.489/0.02 in coniferous forest).
First correlations between pairs of all estimated
parameters, i.e. habitat quality, number of nestlings,
clutch size, laying date, body mass and tarsus lengths,
and condition of adult females and males, were analysed.
Habitat quality, number of nestlings, condition of adult
females and males were found to be statistically uncorrelated parameters. These could be used as effectors
on sex ratio in broods in the generalised linear model.
Laying date, clutch size, body mass and tarsus lengths
statistically correlated with one or more of the above
OIKOS 109:2 (2005)
i)
ii)
iii)
There was no statistically significant impact of
habitat quality and number of nestlings on brood
sex ratio (p /0.57, Table 1). However, male condition correlated positively with a high proportion of
male offspring (p /0.01, Table 1). Although there is
no habitat effect per se, the tendency of habitat
quality influencing brood sex ratio via parental
condition (pfemale /0.04, pmale /0.06, Table 1) may
be assumed.
The differences in body mass between male and
female siblings significantly depended on habitat
quality (pB/0.01, Table 2). Furthermore, nestlings
developed differently in response to habitat quality
(p /0.001, Table 2) and sex ratio (p /0.001,
Table 2).
Differences in body mass between male and female
siblings increased in male-biased broods in the high
quality habitat (p /0.01). However, the low quality
habitat has a negative effect on the sexual dimorphism of siblings in male-biased broods (p /0.02).
369
Table 1. Dependency of sex ratio on habitat quality, number of nestlings, condition of females and males, respectively, in P. major
and P. caeruleus broods. The analysis of variance is based on a generalised linear model (procedure genmod: SAS 1997). The results
of likelihood ratio analyses (type 3) are listed. Significant effects are indicated by/(excess of sons) if high quality habitat and/or
good parental conditions correlate with a male bias. Bold: significant at the 5% level.
Source of variance*
P. major
Habitat quality
Number of nestlings
Male condition
Female condition
Interaction with habitat quality:
number of nestlings
male condition
female condition
deviance
P. caeruleus
sex ratio bias
df
approx. x2
p
df
approx. x2
p
1
1
1
1
4.55
0.22
1.64
3.05
0.033
0.639
0.200
0.081
1
1
1
1
0.32
0.01
7.90
0.92
0.570
0.933
0.005
0.337
1
1
1
84
2.32
0.62
0.00
92.20
0.128
0.429
0.964
1
1
1
72
0.08
3.55
4.07
74.13
0.773
0.059
0.044
male
male
male
*only statistically uncorrelated parameters are considered.
Discussion
Habitat quality determines the physical conditions of
resident individuals. Accordingly, life history traits of
specialist species such as the blue tit (Parus caeruleus )
should be differently affected by environmental variation
than those of sympatrically occurring generalist species
such as the great tit (P. major ).
In the present study, we observed a significant habitat
effect on brood sex ratio for populations of great tits. In
accordance with the hypothesis of Trivers and Willard
(1973), great tit broods from deciduous forests (high
quality habitat) contain more male offspring than those
from the mixed woodland (low quality habitat). Individual condition, however, had no statistically significant
effect on offspring sex ratio.
At first glance, our data seem to contrast the results
obtained by Leech et al. (2001) who did not detect any
correlation between parental quality and offspring sex
ratio in blue tit populations from the UK. However, this
may be due to different analysis procedures. We noticed
that it is crucial to exclude correlated parameters from
the analysis. Otherwise effects can be obliterated, and the
significant correlations described here would have remained undetected.
As food generalists, great tits respond to variation of
resource availability on a population level through
plasticity of life history traits. In contrast, individual-
based response strategies towards habitat quality were
detected for the food specialist blue tit. The condition of
adult males positively correlated to a male-biased sex
ratio. Such correlation of parental body condition and
sex ratio of offspring is also in accordance with the
hypothesis of Trivers and Willard (1973). This hypothesis states that females mating with males in good
condition would increase their fitness by producing
sons rather than daughters. Conversely, females mating
with males in poor condition would invest in daughters.
This was observed in blue tits, tree swallows (Tachycineta
bicolor ) and house wrens (Troglodytes aedon ). In these
species, females in good condition produced male-biased
broods and sons in good condition at the time of
fledging (Svensson and Nilsson 1996, Whittingham
and Dunn 2000, Whittingham et al. 2002). The observation in American (Falco sparverius ) and European (F.
tinnunculus ) kestrels that females in good condition
raised female-biased broods seem to contrast our data.
Yet in these falcons, females are the larger sex demanding more resources (Wiebe and Bortolotti 1992, Korpimäki et al. 2000).
Males of blue tits are found to be the philopatric sex
(Dhondt and Hublé 1968, Greenwood et al. 1979),
suggesting that competition for good territories and
resources is likely to be stronger among males than
females. The assumption that the condition of blue tit
males also mirrors their fitness could explain the female
Table 2. Effect of habitat (coniferous vs deciduous forest) and sex ratio on the development of broods of P. major and P. caeruleus
expressed as the differences in the body mass of male and female offspring. Only broods with more than five nestlings were analysed
(procedure glm, type III; SAS, 1997).
Source of variation
P. major
df
Model
Error
Habitat type
Sex-ratio
Sex-ratio (habitat)
370
3
72
1
1
1
mean square sum
2.174
0.671
1.787
2.384
2.607
P. caeruleus
F-value
p
df
3.24
0.027
2.66
3.56
3.89
0.107
0.063
0.053
3
66
1
1
1
mean square sum
0.733
0.139
1.597
0.111
1.600
F-value
p
5.25
0.003
11.45
0.80
12.62
0.001
0.375
0.001
OIKOS 109:2 (2005)
(a)
Difference in body mass
2.1
Deciduous
Coniferous
1.8
1.5
1.2
0.9
0.6
0.3
0.0
0.0
0.2
0.4
0.6
0.8
1.0
0.8
1.0
Sex ratio
(b)
Difference in body mass
1.4
Deciduous
Coniferous
1.2
1.0
0.8
0.6
0.4
0.2
0.0
0.0
0.2
0.4
0.6
Sex ratio
Fig. 1. Differences in body mass of male and female nestlings in
broods of (a) P. major and (b) P. caeruleus related to sex ratio
and habitat type, respectively. Mean values and standard errors
of body mass differences are presented for five sex ratio classes
(0 /0.2, 0.2 /0.4, 0.4 /0.6, 0.6 /0.8, 0.8 /1.0). The dotted (coniferous) and broken (deciduous) lines depict trends for the
correlation of difference in body mass and sex ratio (non-linear
regression analysis; procedure nlin; SAS, 1997; type one error
for model: pblue tit /0.016, pgreat tit /0.056).
breeding partner’s alteration of the sex allocation.
Sheldon et al. (1999) detected a skewed offspring sex
ratio in blue tits as a female response to male quality
(survival) indicated by ultraviolet plumage ornamentation. Faivre et al. (2003) found that in blackbirds (Turdus
merula ) the secondary sexual traits (bill colour) can
reflect physiological quality such as the status of the
immune system. Our data also indicate that in natural
populations of blue tits individual females can assess the
condition of the mate and react on it by skewing the
offspring sex ratio.
OIKOS 109:2 (2005)
The data presented here revealed no significant
association between female and male condition in
breeding pairs of blue tits. Thus, the generally accepted
view of mate choice being female dominated is
maintained. Additionally, female constitution is relevant
for the sex ratio of the offspring (Table 1). They can skew
the sex ratio and maternally contribute to the fitness of
their offspring. Therefore, the nutritional restrictions
of low quality habitats can act against the advantage of
male-biased sex ratio. Interestingly, we found significantly smaller size differences in blue tit male and
female offspring in male-biased broods (Fig. 1b). This
might be due to the higher energy demand of males for a
normal development that cannot be fulfilled in a low
quality habitat (Stauss et al. unpubl.). Other studies
(Pickering, 1980, Godfray 1986, West et al. 1999, Nager
et al. 2000) have also shown that interactions between
different sexes of offspring can change the sex ratio or
the relative reproductive value of the two sexes. The
consequences of such intra-brood competition were
studied at the population level (Godfray 1986, West et
al. 1999, Werren and Hatcher 2000). However, contextdependent effects of competition between the sexes may
impede the detection of sex ratio adaptation at the
individual level in response to environmental conditions
(West et al. 2002). Finally, paternal effects on sex
ratio might be obliterated when sex dimorphism is not
very pronounced as in the two Parus species (adults
exhibit only /3% sexual dimorphism in mass and size
(males /females, own data). Therefore, larger sample
sizes are necessary in order to demonstrate differences.
Nevertheless, in a recent meta-analysis Sheldon and
West (2004) found greater sex ratio shift in ungulate
species with greater sexual dimorphism. Thus, the
relationships were stronger when sexual size dimorphism
was more male-biased. In the generalist great tit the
results were as expect. A male-bias in offspring is found
in the high quality habitat, regardless of parental
conditions. Conversely, in the specialist blue tit the
overall effect, i.e. good male condition, correlates with
male-biased broods, causing reduced fitness of
male-biased broods in the low quality habitat. Consequently, non-male-biased broods seem to have an
advantage considering the future reproductive value of
offspring.
It has previously been reported that offspring sex ratio
can change in the course of a breeding season (Howe
1977, Blank and Nolan 1983, Clutton-Brock and Jason
1986, Dijkstra et al. 1990, Olsen and Cockburn 1991,
Zijlstra et al. 1992, Daan et al. 1996). For example,
fitness of male fledglings can be reduced when hatching
late in the breeding season due to a lower survival rate
(Nilsson 1989, Dijkstra et al. 1990, Visser and Verboven
1999) and/or a reduced success in settling into a good
territory in the next breeding season (Nur 1984, Tinbergen and Boerlijst 1990, Verboven and Visser 1998, Oddie
371
2000). Thus, in good quality habitats parental fitness
should be highest when producing male offspring in
good condition early in the breeding season. However, in
accordance with other studies (Svensson and Nilsson
1996, Leech et al. 2001) we found no seasonal decline of
the male ratio in both habitats and species.
Our study demonstrates that even closely related
species respond to their environment differently in
adjusting the sex ratio of their offspring in different
habitats. This adaptation is in good congruence with the
theory of sex ratio adjustment
Acknowledgements / We would like to thank J. Blank for
assistance in the field. This work was supported by the Deutsche
Ornithologen-Gesellschaft, the German Academic Exchange
Office No. 313/PPP-N1 and the German Research Foundation
No. DFG To 151/2-1. G.S. was supported by a grant from the
Max-Planck Research Centre for Ornithology. L.B. was
supported in part by the Research Council of Norway
(‘‘National Centre for Biosystematics’’, 146515/420).
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