Behavioral Ecology Vol. 10 No. 6: 659-665
© 1999 International Society for Behavioral Ecology
Fitness components of male and female winter moths (Operophtera brumata L.) (Lepidoptera, Geometridae) relative to measures of body size and asymmetry
a Department of Biology, University of Antwerp (UIA), Universiteitsplein 1, B-2610 Antwerp, Belgium b Department of Ecology, Lund University, S-223 62 Lund, Sweden
Address correspondence to S. Van Dongen, Department of Biology, University of Antwerp (UIA), Universiteitsplein 1, B-2610 Antwerp, Belgium. E-mail: svdongen{at}uia.ua.ac.be .
Received 11 August 1998; revised 1 April 1999; accepted 20 April 1999.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
In this article we present data from two experiments on the association between individual asymmetry and fitness in the winter moth. We performed a mate selection experiment and compared asymmetry and body size of mated and unmated males collected in the field. Individual asymmetry was not associated with copulation probability, adult life span, or body size, even though body size is a reliable indicator of larval and pupal survival, female fecundity, adult life span, and thus expected fitness. There was only a weak positive effect of body size on mating success, contrary to the strong effect of female size on male choice found in previous experiments. Both males and females were capable of repeated mating, and the number of matings was correlated with female size, but neither with male body size nor with adult asymmetry. Yet, females engaged in repeated matings more frequently if they were first mated to a more asymmetrical male. This may indicate that more asymmetrical males lose paternity due to female remating, although direct paternity analyses need to be carried out. In addition, repeated mating may be uncommon under field situations. In conclusion, the relationship between individual asymmetry and fitness seems to be at best weak in the winter moth.
Key words: developmental stability, fitness, fluctuating asymmetry, mate choice, Operophtera brumata, winter moth.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Fluctuating asymmetry (FA), small, random deviations from bilateral symmetry, is assumed to be a measure of an individual's ability to buffer its development against developmental noise (e.g., Palmer and Strobeck, 1992
).
Although many studies have shown a positive relationship between FA and
environmental and/or genetic stress and a negative relationship between
asymmetry and individual quality and fitness, several other studies have
failed to demonstrate such correlations
(Clarke, 1998;
Leung and Forbes, 1996;
Møller and Swaddle,
1997). This heterogeneity between studies may have different
origins. First, individual single-trait asymmetry may only loosely correlate
with developmental instability (Houle,
1997; Van Dongen,
1998b; Whitlock,
1996), such that only relatively weak correlations are expected
and thus often large sample sizes are needed to obtain sufficient statistical
power. Second, the magnitude of FA is often small and may become confounded
with measurement error. Palmer and Strobeck
(1986),
Merilä and
Björklund
(1995), and Van Dongen et al.
(1999), among others, have
argued and shown that the use of within-subject repeats and mixed-model
analysis is required to obtain unbiased estimates of individual asymmetry
values and of population level FA. Third, it has been argued that the
suitability of FA as an estimate of developmental instability may depend on
trait functionality and selection history (e.g.,
Pomiankowski, 1997). Finally,
stress intensities may have to be very strong before they provoke an increase
in FA (Parsons, 1990). Two
recent reviews of the literature have shown that, on average, there is a weak
negative association between individual asymmetry and fitness; however, the
heterogeneity between studies is large and at present poorly understood
(Leung and Forbes, 1996;
Møller, 1997).
Furthermore, a recent evaluation of the studies included in the Møller
(1997) review revealed many
inconsistencies and mistakes (Clarke,
1998). In addition, several recent studies revealed that the
inverse relationship between individual asymmetry and fitness may not be
general (Dufour and Weatherhead,
1997; Markow et al.,
1996; Tomkins and Simmons,
1998).
An interesting open question is what factors affect the relationship
between asymmetry and fitness. In the analysis of the relationship between
individual FA and other factors such as fitness, it is important to
investigate the degree of heterogeneity in developmental instability between
individuals. This can be done by estimating the hypothetical repeatability, a
parameter that estimates the proportion of the total variation in asymmetry
that can be attributed to between-individual variation in developmental
instability (Whitlock, 1996,
1998;
Van Dongen, 1998b). In
addition, within-subject repeats are required to evaluate measurement
accuracy, and sample sizes should be adequately high to have sufficient
statistical power. Ideally, different traits and different fitness components
should be studied.
The population structure of the winter moth on its primary host Quercus
robur L. (Wint, 1983) is
strongly influenced by the degree of synchrony between egg hatching and host
tree budburst phenology (Feeny,
1970; Gradwell,
1974; Van Dongen et al.,
1997; Varley et al.,
1973; Wint, 1983).
Asynchronous hatching results in individuals of smaller size with reduced
expected fitness. The size of an adult has been shown to reflect its degree of
synchrony with an individual host (Van
Dongen et al., 1997,
1998b). Therefore, Van Dongen
et al. (1998b) investigated
male and female mate choice under laboratory conditions and found that males
preferably mate with larger, and thus better synchronized and more fecund,
females. These experiments did not show any patterns of female choice or
male-male competition.
This paper presents results from two experiments studying mate choice in
more detail. Specifically, we monitored copulation behavior of winter moths
over their entire life in the laboratory and collected copulating pairs and
their nearest unmated male in the field. We relate mate success, repeated
mating, and life span to both individual asymmetry and body size. As costs and
benefits of mating and thus the evolution of mating decisions may differ
between the two sexes, we analyzed copulation behavior of both sexes
simultaneously so that patterns can be compared directly (i.e., testing
interactions). Because in many insects and in Lepidoptera in particular,
repeated mating behavior may be influenced or even regulated by spermatophore
size or ejaculate mass (Eisner and
Meinwald, 1995; Raina,
1997; Wiklund and Kaitala,
1993; Wiklund et al.,
1993), we additionally relate repeated mating to male asymmetry
and body size. The winter moth is a good model organism to study the
relationship between asymmetry and mating success because there is a large
amount of variation in individual quality
(Van Dongen et al., 1997,
1998b), which can be expected
to promote the evolution of mate selection patterns.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
The winter moth
The winter moth is a univoltine geometrid moth whose adults are active shortly after dusk in late autumn (November in Belgium). After pupation in the soil, the brachypterous females climb the nearest host tree (Quercus robur L.), where they copulate with the winged males. After copulation the female continues climbing into the canopy, where the eggs are laid. Eggs hatch in spring, and the caterpillars feed for 4-6 weeks before dropping to the ground on a silk thread for pupation (Feeny, 1970
;
Varley et al., 1973).
Experiment 1
We performed a mate selection experiment under laboratory conditions with
reared winter moths. Copulating winter moth pairs (a total of 32 pairs) were
collected in November 1996 in several oak forests near Antwerp in northern
Belgium. A full description of the study area is given in Van Dongen et al.
(1998a). Females were allowed
to lay eggs on a paper roll over the next 5-6 days. Eggs were stored outdoors
and hatching caterpillars were fed with fresh oak leaves the next spring. We
stored pupae individually in Eppendorf tubes covered with 2 cm of soil to
prevent dehydration. In mid-September 1997, pupae were transported to Lund
(Sweden) and placed in larger glass jars. We checked pupal eclosion daily, and
only newly emerged adults were used for the experiment.
The mate selection experiment was performed in a cooled room (10°C)
with an 8 h:16 h light:dark cycle. We recorded the mating behavior of 80 males
and 68 females over their entire life. Each day, we randomized 24 males over
24 plastic trays (30 x 22 x 12 cm), each of which contained 1
female, at least 1 h before the start of the observations. For each
male/female combination, we recorded if they copulated or not. After darkness,
observations were made continuously for the first hour, and afterward
observations were made every 15 min over 3-5 h. As most copulations are
expected to occur during the first hour and last between 1 and 5.5 h
(Alma, 1970), we should have
missed very few matings (see also Van
Dongen et al., 1998b). Dead individuals were replaced by newly
emerged adults each day. All dead individuals were stored at -80°C before
measurement.
We estimated individual life span and number of copulations, which we
correlated with individual asymmetry and body size. The probability of
copulation for each individual during a single night was analyzed in relation
to male and female asymmetry, body size, age, and previous copulation behavior
(copulated before or not) using a logistic regression model with logit link
function and binomial error structure. As the effects of these factors may
differ between males and female, the interaction with sex was tested as well.
Because repeated observations per individual were made, the correlation
between repeated measurements needed to be modeled. Each copulation event
contributed to two observations (i.e., one for the male and one for the
female) in this analysis, because both sexes were analyzed simultaneously.
Therefore, we modeled the correlation structure separately for males and
females using the GLIMMIX macro of SAS software (version 6.12; GROUP option
for the REPEATED statement). This macro applies a quasi-likelihood approach
(Wedderburn, 1974) to estimate
the different parameters of the model. A compound symmetry (i.e., equal
within-individual correlation between the residuals) as well as a first-order
autoregressive (i.e., within-individual correlation between the residuals
equal to 
, where represents the number of days
between the two observations) correlation structure was estimated and compared
with an unstructured (i.e., no mathematical pattern imposed on the covariance
matrix) variance-covariance matrix to select the appropriate correlation
structure. Degrees of freedom were estimated according to Satterthwaite's
formula (see Littell et al.,
1996; Verbeke and Molenberghs,
1997, for more details on the SAS procedures). As a consequence,
degrees of freedom cannot be recalculated from sample sizes and number of
factors in the model and may vary depending on the correlation structure. The
GLIMMIX macro models the dependence of the data and estimates the appropriate
degrees of freedom for the nonnormally distributed error term (binomial
distribution in this case) (Littell et
al., 1996). All analyses were performed using SAS software
(version 6.12), and all significance levels are two-tailed unless otherwise
noted.
To avoid presentation of large tables with correlation coefficients and significance tests, for this experiment we only report the analyses for an average individual asymmetry measure based on the asymmetry values of the three tibias (see below). Analyses with the single-trait FA values were also performed and gave similar results.
The unsigned asymmetry is typically half-normally distributed. As a result,
it has a long right-hand tail. In analyses based on parametric methods, the
observations in the tail of the distribution will become influential and may
bias the outcome (but see Gangestad and
Thornhill, 1998). Therefore, we used a log transformation of this
unsigned asymmetry in all parametric analyses, which normalized the data well
as judged from the Shapiro-Wilks statistics (W > 0.95).
Experiment 2
In November 1996 and 1997, copulating pairs as well as the nearest single
male (closer than 1 m) were collected in Belgium and Sweden, respectively. The
two Belgian study sites were a large (>200 ha; n = 68 pairs +
single male) and a small (2 ha; n = 44 pairs + single male) forest
near Antwerp (PB and KL, respectively, in
Van Dongen et al., 1998a). The
Swedish study site (Linnebjär; n = 65
pairs + single male) was an oak forest with a size of approximately 50 ha.
This area was located a few kilometers northeast of Lund. All moths were
collected by hand on oaks between 1700 and 2000 h. They were transported in
plastic trays and stored at -80°C until measurement.
We compared average asymmetry, single trait asymmetry, and body size between successful and unsuccessful males. Assortative mating for both asymmetry and body size was analyzed by Spearman rank correlations. The effect of asymmetry and/or body size on male mating success may depend on female asymmetry and/or body size as well. To investigate this, we correlated the difference in individual male asymmetry and in male body size of the successful and unsuccessful males with female asymmetry and body size. If, for example, larger females would mate preferably with more symmetrical males, while relatively smaller females would show no preference, a negative correlation would be expected. We tested correlations between body size and individual asymmetry for males and females separately. In all analyses samples from Belgium and Sweden were pooled, but differences in body size between the two countries were corrected for (PARTIAL option in SAS software). Analyses per country gave similar results.
To investigate repeated mating in the field, we dissected all females and counted the number of spermatophores in their bursa copulatrix. We also measured spermatophore length and maximum width to the nearest 0.01 mm under a microscope and correlated these with male asymmetry and body size. In case more than one spermatophore was present, we used the one with the collum in the ductus bursae. If two or more collums appeared in the ductus bursae, these data were not included in the correlation analysis.
Measurement of asymmetry and body size
Asymmetry was measured for the tibia of the three pairs of legs (1: front;
2: middle; 3: back) of both males and females. For the males of experiment 2,
front wing asymmetry was measured as well. Unfortunately, many of the males in
experiment 1 showed incomplete wing unfolding, probably as a result of the
environment in which they pupated. Therefore, the wing asymmetry could not be
measured accurately for these individuals. Legs and wings were removed and
pressed between two glass slides for measuring. In this way tibias were
flattened and we eliminated measurement error (ME) due to bending of the legs
during storage in Eppendorf tubes. We did not remount the tibias between two
successive measurements because this sometimes damaged them. We thus
implicitly assume that the mounting process itself did not introduce much ME
or bias, and that ME due to bending, which we eliminated by mounting the legs,
was much larger. We mounted all legs in the same direction and such that they
were pressed laterally between the glass slides. The length of the tibias as
well as the length of a vein in the front wing (A-B in
Van Dongen, 1997) was measured
under a microscope to the nearest 0.033 mm. Two independent repeats on both
sides were obtained to allow mixed model analysis and separation of asymmetry
due to ME and due to real FA (Palmer and
Strobeck, 1986), as well as to model and test heterogeneity in FA
and ME (Van Dongen et al.,
1999). Body size was expressed as the average of mean tibia length
(averaged over all repeats and tibia) and wing length (for males) or body
length (for females). Wing length and body length were measured to the nearest
0.1 mm. We chose to use this average of the two size measures because both
were strongly correlated (males: r =.68, n = 80, p
<.0001; females: r =.46, n = 68, p <.0001).
Before averaging, mean tarsus length and wing (or body) length were
standardized by subtraction of their respective means and division by their
standard deviations.
We calculated single-trait individual asymmetry by averaging within-subject
repeats for the three tibias (left minus right average trait size; i.e.,
signed FA). The distribution of the signed FA was tested for normality using
the Shapiro-Wilks test, and the hypothetical repeatability was estimated
following Van Dongen (1998a;
see Table 1 for formula). All
core analyses were based on the absolute values of these signed asymmetries
(i.e., unsigned FA). Average individual asymmetry was calculated as the mean
of the standardized single-trait asymmetry values.
|
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Distribution, significance, and hypothetical repeatability of asymmetry
Summary statistics and hypothetical repeatability of the asymmetry of the different traits are given in Table 1. The variance components as obtained from a mixed regression model showed that body size variation was high relative to variation due to FA. Fluctuating asymmetry made up between 5% and 35% of the total variation. Measurement error was always an order of magnitude smaller than FA, indicating accurate measurement. Consequently, FA was highly significant for all traits (all p <.001). After sequential Bonferonni correction, there were no significant differences in FA between animals collected in Belgium and Sweden. Analyses were performed for males and females separately, as previous investigations have indicated significant between-sex differences (Van Dongen et al., manuscript in preparation), but pooled analyses gave similar results. Because the maximal value of the hypothetical repeatability (R) is 0.637 (Whitlock, 1998
), the
observed values of R were generally quite high, except for wing vein
length and for tibia 3 in the females of experiment 2. This means that
between-individual variation in the presumed underlying developmental
instability is large, assuming that there is no antisymmetry
(Van Dongen, 1998a).
Unfortunately, it is not possible to separate population mixture of different
levels of individual developmental stability and a mixture of real FA and
antisymmetry statistically because both result in a leptokurtic distribution
of the signed FA (Gangestad and Thornhill,
1999; Palmer and Strobeck,
1992; Van Dongen,
1998a). The distribution of the signed FA in this study appeared
to deviate significantly from normality for all traits in both experiments
except for tibia 3 in experiment 1 (W = 0.98, n = 62,
p =.67) and for male wing asymmetry (W = 0.98, n =
344, p =.4). All deviations from normality appeared to be the
consequence of leptokurtisis.
Experiment 1
Males lived, on average, 1 day less than females [males: 7.8 days (SD =
2.6); females: 8.8 days (SD = 4.8); Mann-Whitney U test: z =
2, p =.05]. Life span was not significantly correlated with average
individual asymmetry (AIA; males: rs = -.11, n =
80, p =.4; females: rs = 0.2, n = 65,
p =.1) but was significantly correlated with body size for males
(rs = 0.41, n = 80, p <.001) and
females (rs =.28, n = 65, p =.02). Males
and females copulated, on average, 1.0 (SD = 1.2) and 1.2 (SD = 1.0) times,
respectively, over their life span with no significant difference
(Mann-Whitney U test: z = 1.3, p =.2). The number
of copulations was not correlated with AIA (males: rs =
-0.09, n = 80, p =.4; females: rs =
0.10, n = 61, p =.4) but was significantly correlated with
female (rs = 0.27, n = 61, p =.04), but
not male (rs = 0.16, n = 80, p =.14),
body size. The number of copulations ranged between 0 and 5 for both sexes.
The proportions of males and females copulating 0-5 times were 41, 26, 16, 12,
4, and 1% for the males, and 30, 43, 23, 2, 1, and 1% for the females. The AIA
was not correlated with body size (males: rs = -0.09,
n = 80, p =.4; females: rs = 0.22,
n = 61, p =.1).
The copulation probability of each individual during each night was analyzed with a logistic regression model with correlated error structure. As the unstructured correlation structure showed little variation among the different covariances corresponding to observations separated by different number of days, we selected a compound symmetry structure over the first-order autoregressive structure to model the dependence of the repeated measurements. Nevertheless, both structures gave similar results. For males, the within-individual correlation between the residuals of two observations was.02 (SE = 0.035, Z = 0.62, p =.53), whereas it was.07 (SE = 0.04, Z = 1.68, p =.09) for the females. These low nonsignificant correlations indicate that repeated observations within the same individual are nearly independent. Nonetheless, we continued our analyses, keeping these correlation structures in the model, because eliminating a non-zero correlation could bias the outcome of the fixed effect tests. Table 2 summarizes the significance tests of the different factors. The probability of copulation decreased with age, and this relationship (parameter estimate = -1.08, SE = 0.19, t813 = -5.6, p <.0001) was the same for both males and females (no significant age x sex interaction). There was a nonsignificant trend for copulation probability during a single night to increase with adult size, and, again, this relationship (parameter estimate = 0.22, SE = 0.12, t103 = 1.8, p =.07) did not differ between males and females (no significant size x sex interaction). It is important to note that the relationship for males and females separately was not statistically significant (males: parameter estimate = 0.28, SE = 0.17, t41 = 1.65, p =.11; females: parameter estimate = 0.18, SE = 0.18, t57 = 0.99, p =.33). The effect of previous matings (i.e., individual previously mated or not) differed between the two sexes (highly significant copulation before x sex interaction). Males that had mated earlier had a higher copulation probability [difference in parameter estimates (mated-not mated before) = 0.58, SE = 0.29, t183 = -2.0, p =.04; Figure 1]. For females the copulation probability decreased if a mating had occurred before [difference in parameter estimates (mated-not mated) = -1.44, SE = 0.30, t318 = 4.8, p <.0001; Figure 1]. There was no correlation between AIA and copulation probability for any of the sexes (Table 2).
|
|
Of the females, 29% (20 out of 68) were involved in repeated matings. We used logistic regression to model the probability of a first mating being followed by a second mating in relation to body size and asymmetry of the first male. The probability increased with male AIA (parameter estimate = 0.74, SE = 0.33, z = 2.26, p =.02) but was not correlated with male body size (parameter estimate = 0.04, SE = 0.39, z = 0.12, p =.91). We also modeled the probability that any mating of a female (first or repeated) was followed by an additional mating. Similarly, this probability increased with male AIA (parameter estimate = 0.46, SE = 0.23, z = 2.03, p =.04) but was independent of male body size (parameter estimate = -0.04, SE = 0.35, z = -0.11, p =.90).
Experiment 2
Average and single-trait asymmetry as well as body size did not differ
between the successful and unsuccessful males (all p >.3;
Figure 2). There was no
evidence for assortative mating for body size (r =.06, n =
177, p =.4) and asymmetry (all p >.1 for the correlations
of single-trait and average asymmetry). Nor were there any correlations
between female asymmetry (average and single trait) and the difference in both
male asymmetry (average and single trait) and male body size between the
successful and unsuccessful individuals (all p >.2).
|
Out of 177 dissected females, eight (5%) contained two and two (1%) contained three spermatophores. In one female no spermatophore was found. The frequency of repeated matings in the field (6%, 10 out of 177) was significantly lower than the frequency in the laboratory (29%, 20 out of 68, see above; Fisher's Exact test: p <.0001) but did not differ between moths collected in Sweden and Belgium (Sweden 9%, 6 out of 65; Belgium 4%, 4 out of 112; Fisher's Exact test: p =.17). Because spermatophore length and maximal width were highly correlated (r =.87), we used the average as an estimate of spermatophore size. The correlation between spermatophore size and both single-trait and average male asymmetry was statistically nonsignificant (tibia 1: rs = -.08, n = 168, p =.3; tibia 2: rs = -0.10, n = 168, p =.2; tibia 3: rs = -0.08, n = 166, p =.3; wing vein: rs = -0.02, n = 168, p =.8; AIA: rs = -0.10, n = 156, p =.2). Male body size was weakly positively correlated with spermatophore size (rs = 0.17, n = 171, p =.04).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
This study does not support any relationship between individual asymmetry and life span or mating success for either males or females. This result is unlikely to be attributable to low sample sizes or to a low hypothetical repeatability of individual asymmetry. Furthermore, measurement error was much lower compared to FA, and two within-subject repeats were obtained for all individuals and traits. In addition, the use of average asymmetry values taken over the three or four traits did not result in any significant associations with these fitness traits. Thus, individual asymmetry does not seem to be correlated with these two fitness components in the winter moth. Furthermore, this and previous work has revealed that body size, which is a reliable indicator of degree of local adaptation to the phenology of individual hosts (Van Dongen et al., 1997
),
female fecundity (Embree, 1965;
Van Dongen, 1997), female
mating success (Van Dongen et al.,
1998b; but see below), survival probability during pupation
(Gradwell, 1974), and male and
female life span (this study), was not related to individual asymmetry either
(Van Dongen, 1997).
We did find indications that females might influence the paternity of their
offspring by repeated mating, such that more symmetrical males could father
more offspring. The probability that a first mating of a female was followed
by one or more repeated matings increased with the asymmetry of the first male
but was not correlated with male body size. Furthermore, a mating of a female
had a higher probability of being the last mating if the asymmetry of that
male was relatively low. Again, there appeared to be no correlation with male
body size. Because in most Lepidoptera the last male to copulate with a female
fathers a significantly higher proportion of the offspring
(Drummond, 1984;
Gwynne, 1984), this pattern of
repeated mating could indicate that more symmetrical males may father more
offspring (but see Drummond,
1984; LaMunyon,
1994). Therefore, direct paternity analyses have to be carried out
for the winter moth. Even if paternity is shared equally between males,
asymmetric males lose paternity due to the higher number of matings by the
female. In addition, in 6 out of the 10 cases where more than 1 spermatophore
was found in the female's bursa copulatrix, the collum of only 1 spermatophore
was still present in the ductus bursae. This indicates that the spermatophore
of the first male(s) was displaced by the one from the last male, which is
likely to reduce the probability of paternity
(Drummond, 1984). The positive
correlation between total number of matings and female body size might
indicate that larger females are more selective compared to the smaller ones
or that smaller females have a shorter life span and therefore less time and
opportunity to obtain repeated matings.
Multiple mating may be the only way female winter moths can influence the
paternity of their offspring. Female moths typically emit pheromones to
attract males, and these signals cannot be directed to particular potential
mates (Svensson, 1996; but see
Greenfield, 1981). As male
winter moths do not court females before mating, females may not be able to
resist male mating attempts and/or may have no information on the quality of
the attempting male. Assuming that females can influence the paternity of
their offspring by repeated matings, it remains unclear what male asymmetry
expresses, and what benefits females may have from repeated matings. Male (as
well as female) asymmetry was not correlated with individual size (see also
Van Dongen, 1997), whereas
size is a reliable indicator of degree of local adaptation and female
fecundity, and males appeared to preferentially mate with larger females if
given the choice (Van Dongen et al.,
1998b; but see below). Possibly, male asymmetry is correlated with
some other trait, such as successful placement of the spermatophore, that may
be of more benefit to the female. Furthermore, in many Lepidoptera, the male
spermatophore contains nutrients that can be used by the females for egg
production (Drummond, 1984).
However, we found no indications that more symmetrical males tended to produce
larger spermatophores, although spermatophore size was positively, but weakly,
correlated with male size, and this factor did not appear to influence
repeated mating by females. Pheromone production in female moths of some
species has been shown to decrease after mating under the influence of
peptides produced by male accessory glands
(Raina, 1997), so other
characteristics of the male spermatophore might be correlated with asymmetry.
For example, as already mentioned, asymmetry may be positively associated with
poor spermatophore placement, which in turn may lead to nondrainage of the
pheromones that decrease or cause cessation of female receptivity. In this
scenario female remating is a consequence of the poor quality of the previous
mate but does not invoke any choosiness.
Although female remating occurred relatively frequently in the laboratory
experiment we performed, it may be less common in the field. Under natural
conditions, males copulate with females on the lower parts of the trunk, after
which females climb into the canopy to lay eggs
(Briggs, 1957). The movement of
males upward during the course of the night
(Alma, 1970) may be adaptive.
During the first hours of the night, males stay on the lower parts of the
trunk trying to copulate with the emerging virgin females. After about 2 h
this female activity drastically decreases (Alma, 1997; Van Dongen S,
unpublished data), and males might attempt to mate with already mated females
active in the canopy.
In conclusion, this study provides no evidence for a strong relationship
between individual asymmetry and fitness and supports the growing awareness
that such a correlation may not be ubiquitous (see also
Clarke, 1998;
Dufour and Weatherhead, 1997;
Leung and Forbes, 1996;
Markow et al., 1996;
Tomkins and Simmons, 1998).
Examining four fitness components, we found indications that only one of them
was related to asymmetry—namely, that male asymmetry is related to
female remating behavior. Furthermore, it is not clear if male asymmetry is
related to any quality trait, either direct or indirect, at all. The fact that
individual asymmetry may be related to only a few of many possible fitness
traits in some species may be an important factor contributing to
heterogeneity between different studies.
|
ACKNOWLEDGEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
S.V.D. is research assistant, and E.M. is a research associate with the Fund for Scientific Research—Flanders (FWO). We thank Geert Molenberghs for his help with the statistics and two anonymous reviewers for their constructive comments on earlier versions of the manuscript. This work was partially funded by the Knut and Alice Wallenberg Foundation and the Swedish Natural Science Research Council.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Alma PJ, 1970. A study of the activity and behaviour of the winter moth, Operophtera brumata (L.) (Lep., Hydriomenidae).Entomol Mon Mag 105:258-265.
Briggs JB, 1957. Some features of the biology of the winter moth (Operophtera brumata (L.)) on top of fruits. J Hort Sci 32:108-125.
Clarke GM, 1998. Developmental stability and fitness: the evidence is not quite so clear. Am Nat 152:762-766.
Drummond III BA, 1984. Multiple mating and sperm competition in the Lepidoptera. In: Sperm competition and the evolution of animal mating systems (Smith RL, ed). Orlando, Florida: Academic Press; 291-370.
Dufour KW, Weatherhead PJ, 1997. Reproductive consequences of bilateral asymmetry for individual male red-winged blackbirds.Behav Ecol 9:232-242.
Eisner T, Meinwald J, 1995. The chemistry of sexual selection. In: Chemical ecology: the chemistry of biotic interaction (Eisner T, Meinwald J, eds.). Washington, DC: National Academy Press; 119-132.
Embree DG, 1965. The population dynamics of the winter moth in Nova Scotia, 1954-1962. Mem Entomol Soc Can 46:1-57.
Feeny P, 1970. Seasonal changes in oak leave tannins and nutrients as a cause of spring feeding by winter moth caterpillars.Ecology 51:565-581.
Gangestad SW, Thornhill R, 1998. The analysis of fluctuating asymmetry redux: the robustness of parametric statistics.Anim Behav 55:497-501.[ISI][Medline]
Gangestad SW, Thornhill R, 1999. Individual differences in developmental precision and fluctuating asymmetry: a model and its implications. J Evol Biol 12:402-416.
Gradwell GR, 1974. The effects of defoliators on tree growth. In: The British oak. Its history and life history (Morris MG, Perring FH, eds). Flaringdon, UK: Classey for the Botanical Society of the British Isles; 182-193.
Greenfield MD, 1981. Moth sex pheromones: an evolutionary perspective. Fla Entomol 64:4-17.
Gwynne TG, 1984. Male mating effort, confidence of paternity, and insect sperm competition. In: Sperm competition and the evolution of animal breeding systems (Smith RL, ed). Orlando, Florida: Academic Press; 117-151.
Houle D, 1997. Comment on `A meta-analysis of the heritability of developmental stability' by Møller & Thornhill.J Evol Biol 10:17-20.
LaMunyon CW, 1994. Paternity in naturally-occurring Uthetheisa ornatrix (Lepidoptera: Arctiidae) as estimated using enzyme polymorphism. Behav Ecol Soc 34:403-408.
Leung B, Forbes MR, 1996. Fluctuating asymmetry in relation to stress and fitness: effect of trait type as revealed by meta-analysis. Ecoscience 3:400-413.
Littell RC, Milliken GA, Stroup WW, Wolfinger RD,1996 . SAS system for mixed models. Cary, North Carolina: SAS Institute.
Markow TA, Bustoz D, Pitnick S, 1996. Sexual selection and a secondary sexual character in two Drosophila species. Anim Behav 52:759-766.
Merilä J, Björklund M, 1995. Fluctuating asymmetry and measurement error. Syst Biol 44:97-101.
Møller AP, 1997. Developmental stability and fitness: a review. Am Nat 149:916-932.[ISI]
Møller AP, Swaddle JP, 1997. Asymmetry, developmental stability, and evolution. New York: Oxford University Press.
Palmer AR, Strobeck C, 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391-421.[ISI]
Palmer AR, Strobeck C, 1992. Fluctuating asymmetry as a measure of developmental stability: implications of non-normal distributions and power of statistical tests. Acta Zool Fenn 191:57-72.
Parsons PA, 1990. Fluctuating asymmetry and stress intensity. Trends Ecol Evol 5:97-98.
Pomiankowski A, 1997. Genetic variation in fluctuating asymmetry. J Evol Biol 10:51-55.
Raina AK, 1997. Control of pheromone production in moths. In: Insect pheromone research: new direction (Cardé RT, Minks AK, eds). New York: Chapman & Hall.
Svensson M, 1996. Sexual selection in moths: the role of chemical communication. Biol Rev 71:113 -135.
Tomkins JL, Simmons LW, 1998. Female choice and manipulations of forceps size and asymmetry in the earwig Forficula auricularia L. Anim Behav 56:347 -356.
Van Dongen S, 1997. The population structure of the winter moth (Operophtera brumata L.) in relation to local adaptation and habitat fragmentation (Ph.D. dissertation). Antwerp: University of Antwerp.
Van Dongen S, 1998a. The distribution of individual asymmetry: why are the coefficients of variation of the unsigned FA so high?Ann Zool Fenn 35:79-85.
Van Dongen S, 1998b. How repeatable is the estimation of developmental stability by fluctuating asymmetry? Proc R Soc London B 265:1423-1427.
Van Dongen S, Backeljau T, Matthysen E, Dhondt AA,1997 . Synchronization of hatching date with budburst of individual host trees (Quercus robur) in the winter moth (Operophtera brumata) and its fitness consequences. J Anim Ecol 66:113-121.
Van Dongen S, Backeljau T, Matthysen E, Dhondt AA,1998a . Genetic population structure of the winter moth (Operophtera brumata L.) (Lepidoptera, Geometridae) in a fragmented landscape. Heredity 80:92-100.
Van Dongen S, Matthysen E, Sprengers E, Dhondt AA,1998b . Mate selection by male winter moths Operophtera brumata (Lepidoptera, Geometridae): adaptive male choice or female control? Behaviour 135:29-42.
Van Dongen S, Molenberghs G, Matthysen E, 1999. Statistical analysis of fluctuating asymmetry: REML estimation of a mixed regression model. J Evol Biol 12:94-102.
Varley GC, Gradwell GR, Hassell MP, 1973.Insect population ecology . Oxford: Blackwell Scientific.
Verbeke G, Molenberghs G, 1997. Linear mixed models in practice: a SAS-oriented approach. Lecture notes in statistics 126. New York: Springer-Verlag.
Wedderburn RWM, 1974. Quasi-likelihood methods,
generalised linear models, and the Gauss-Newton method.Biometrika
61:439-447.
Whitlock M, 1996. The heritability of fluctuating asymmetry and the genetic control of developmental stability. Proc R Soc Lond B 263:849-854.[Medline]
Whitlock M, 1998. The repeatability of fluctuating asymmetry: a revision and extension. Proc R Soc Lond B 265:1429-1431.
Wiklund C, Kaitala A, 1993. Sexual selection for large male size in a polyandrous butterfly: the effect of body size of male versus female reproductive success in Pieris napi. Behav Ecol 6:6-13.
Wiklund C, Kaitala A, Lindfors V, Abenius J, 1993. Polyandry and its effect on female reproduction in the green-veined white butterfly (Pieris napi L.). Behav Ecol Soc 33:25-33.
Wint W, 1983. The role of alternative host-plant species in the life cycle of a polyphagus moth, Operophtera brumata (Lepidoptera: Geometridae). J Anim Ecol 52:439-450.
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||