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Behavioral Ecology Vol. 10 No. 5: 498-503
© 1999 International Society for Behavioral Ecology
Wing length and asymmetry of male Tokunagayusurika akamusi chironomid midges using alternative mating tactics
National Institute for Environmental Studies, 16-2 Onogawa, Tukuba, Ibaraki 305-0053, Japan
Address correspondence to K. Takamura. E-mail: takaken{at}nies.go.jp .
Received 4 September 1998; revised 6 January 1999; accepted 31 January 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male Tokunagayusurika akamusi chironomids have alternative mating tactics. One is to search for females on vegetation (ground mating), and the other is to wait for females in an aerial swarm (swarm mating). Simultaneous sampling of ground-unpaired and ground-paired males and of swarm-unpaired and swarm-paired males were performed. The average wing length and right-left wing length difference (wing asymmetry) were compared between males from the four different categories. Swarm-unpaired males were larger than ground-unpaired ones, swarm-paired males were larger than swarm-unpaired ones, and ground-paired males were not larger than ground-unpaired ones. Thus, large males tended to aggregate in swarms, and larger swarming males mated more successfully. On the other hand, small males probably enjoyed mating on the ground, especially when large males swarmed. The wing asymmetry was not significantly different between unpaired and paired males both within and between tactics. There was a flat or U-shaped relationship between wing length and asymmetry, underpinning the lack of a symmetrical advantage of swarming to large males. The right-left difference was not normally distributed in four of six samples of unpaired males but, in contrast, was not normally distributed in only one of six samples of paired males. The non-normal distributions were leptokurtic and included outliers. Removal of the outliers improved normality, suggesting that males with extremely asymmetric wings were not successful in mating.
Key words: chironomids, alternative mating tactics, fluctuating asymmetry, normal distribution, outliers, swarm, Tokunagayusurika akamusi, wing length.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Male animals compete for acquisition of female mating partners. Generally, as a result of this competition, some males achieve a higher rate of mating success than others. Sexual selection favors male traits that increase the individual's competitive ability. Size is probably the most commonly studied trait to discriminate between successful and unsuccessful males. Large size is often correlated with increased fighting ability (e.g., Alcock, 1966a
,
b;
Thornhill and Alcock, 1983),
or some other characteristics, like longevity and endurance, related to mating
performance. On the other hand, small size is advantageous in achieving higher
mating success as a result of greater agility (e.g.,
McLachlan and Cant, 1995;
Steele and Partridge, 1988).
Consequently, large and small males of the same species sometimes have
different mating tactics (e.g., Arak,
1988; Gross,
1985).
Recently, fluctuating asymmetry (FA) has been used as a predictor of male
mating success (Leung and Forbes,
1996; Møller,
1992; 1997;
Palmer and Strobeck, 1986;
Simmons, 1995;
Thornhill, 1992a,
b). There has been much
controversy concerning the role of FA as a reliable indicator of male mating
ability (Eggert and Sakaluk,
1994; Markow,
1995; Van Valen,
1962). It is plausible that reliability depends on which character
is measured because characters play roles of differing importance during
mating. As long as appropriate characters are measured, it is likely that the
magnitude of asymmetry indicates the individual's quality
(Eggert and Sakaluk, 1994;
Møller and Hoglund,
1991; Møller and
Pomiankowski, 1993b) or, alternatively, asymmetry may affect
performance during mating (Allen and
Simmons, 1996; McLachlan and
Cant, 1995).
Male chironomid midges (Diptera) have two main mating tactics: swarming and
searching (reviewed by Armitage,
1995; Kon, 1987).
In swarming, a columnar aggregation of males is formed in the air. Searching
is performed by looking for females on the ground. Many chironomid species
have been reported to use one of these strategies, in most cases swarming
(reviewed by Armitage, 1995).
For example, the chironomid Chironomus plumosus mates by swarming
(McLachlan and Cant, 1995). In
this species, small males mate more successfully and have less FA in wing
length. Small males may have greater agility in the air, giving them an
advantage in finding mates in the swarm.
Males of the chironomid Tokunagayusurika akamusi use both swarming
and ground searching as alternative tactics
(Kon et al., 1986;
Sasa, 1978). Both tactics
occur in the same population, but generally at different times of the day
(Kon et al., 1986). Searching
males on the ground are commonly observed in the morning, whereas swarming
males are seen in the afternoon. Flight ability may strongly influence male
competitive ability within swarm mating, but may be less important in search
mating. If wing length is directly associated with flight ability, as
advantageous positioning in swarms of love bugs
(Thornhill, 1980), wing length
should be greater in successful swarming males. In the same way, if wing
asymmetry is directly associated with flight ability, as in birds
(Thomas, 1993), then wing
asymmetry should be lower in successful swarming males. Moreover, there should
be no difference in wing asymmetry between successful and unsuccessful males
adopting the ground-searching tactic. In this study, I compared both wing
asymmetry and wing length.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Tokunagayusurika akamusi spend the larval and pupal stages in eutrophic lakes. Adult midges emerge and mate for the period of about 1 month in late fall (Iwakuma, 1987
;
Iwakuma and Yasuno, 1983;
Iwakuma et al., 1989;
Yamagishi and Fukuhara, 1971).
During this period, mating generally occurs on the ground in the morning and
in aerial swarms in the afternoon (Kon et
al., 1986). Emergence of midges is concentrated in the 2 h just
after sunset (Iwakuma and Yasuno,
1983), and fresh individuals appear on the riparian vegetation in
the morning (Kon et al.,
1986).
Midges were caught on the shore of Lake Kasumigaura, central Japan. In the
morning, male midges copulating with females on the ground (ground-paired
males) were hand collected into 2-ml plastic tubes from the vegetation such as
Phragmites communis and Solidago altissima. Simultaneously,
males not copulating were caught from the vegetation by net sweeping
(ground-unpaired males). The proportion of searching males to total number of
males on the ground changes with time; however, almost all males on the ground
perform searches for female partners at the time of peak activity in the
morning (Kon et al., 1986).
The males swept from the vegetation included one or two males copulating with
females. They were not avoided during sweeping, because their exclusion might
have hindered a random sampling of males at a site.
Male midges formed swarms up to a height of 10 m or more. Once a male succeeded in copulating with a female, the pair left the swarm and flew down to the ground. While copulating with females, males were trapped on a white cotton sheet spread on the ground just beneath a swarm. Alternatively, they were caught with an insect net while flying (swarm-paired males). Males that did not copulate and hovered in the same swarm were netted with an insect net when the swarm was swept down toward the ground by a strong breeze (swarm-unpaired males).
I performed each of the above sampling procedures three times on different dates, resulting in three pairs of samples for each mating tactic. Unpaired males were anesthetized with ethyl acetate soon after collection and kept in a freezer. Each pair of copulating males and females was put in a 2-ml plastic tube and kept in a freezer.
I removed both wings from each male midge and placed them under a glass cover slip on a glass slide with the dorsal side up. Wing lengths were measured to the nearest 0.001 mm using image analysis with the aid of image-analyzing software (Mac Scope, version 2.2.1, Mitani Corp.) installed on a Macintosh 8100/100AV with a PC-aided digital camera (HC-1000, Fujifilm, Tokyo) mounted on a stereoscopic microscope. The magnification was about 25 x. I measured wing length as the distance between the antero-proximal corner of the first basal cell (r) and the postero-distal corner of the first submarginal cell (r2+3). I calculated the average length and right-left difference in wing length for each midge.
I repeated length measurements at least twice per wing to evaluate the
repeatability of measurements of right-left difference in wing length. The
measurements were tested using a two-way mixed-model ANOVA
(Palmer and Strobeck, 1986).
The measurement error was significantly less than the difference in all 12
samples tested (p <.0001, the highest probability at
F60,122 = 18.0), indicating high repeatability of the
measurements.
The average length and unsigned (transformed into absolute values)
right-left differencess were compared among each three samples of
ground-unpaired, ground-paired, swarm-unpaired, or swarm-paired males using
Kruskal-Wallis tests. When the values were not significantly different among
the three samples, I pooled the samples. When values were significantly
different among the samples, they were not pooled. Further comparisons between
these categories of males were made using Mann-Whitney U tests.
Because the minimum number of males in one sample was 22, the statistic
Z was calculated instead of U
(Zar, 1996) in all
Mann-Whitney U tests. Because pooling three samples was inadequate
for wing length of swarm-paired males (see Results), I compared wing length
within each pair of swarm-unpaired and swarm-paired males. Under the null
hypothesis that there is no significant difference in wing length between
these males, the significance level was adjusted to 0.017 after Bonferroni
correction, as there were three paired comparisons for the null
hypothesis.
To assess the relationship between wing length and right-left difference, I averaged unsigned differences of the all samples of ground- and swarm-unpaired males for wing length classes in 0.1-mm intervals and performed regression analysis against the length.
Asymmetrical right-left differences in wing length were confirmed as FA if
the signed difference in right and left wing length was normally distributed
and did not differ significantly from a mean value of 0 (see
Swaddle et al., 1994). To
confirm normality, I tested the signed values of the difference using the
method of Filliben (1975). In
addition, to test the zero mean, the signed values were tested using a
one-sample t test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Mean wing length of male midges in each sample ranged from 4.90 to 4.99 mm, with a maximum value of 5.38 mm and a minimum of 4.37 mm in the whole of the samples. Wing length was not significantly different among ground-unpaired, swarm-unpaired, and ground-paired males (Kruskal-Wallis test with tied ranks, H = 2.30, p =.32; H = 1.71, p =.43; H = 3.45, p =.18, respectively), but was significantly different among the samples of swarm-paired males (H = 6.48, p =.04). Consequently, the former three sets of samples were pooled for further comparisons.
Wing length was significantly different between ground- and swarm-unpaired males (Mann-Whitney U test, Z = -4.87, p <.001). Swarm-unpaired males (mean ± SD = 4.98±0.146 mm) were larger than ground-unpaired ones (4.92±0.148 mm). Wing length was not significantly different between ground-unpaired and ground-paired males (Mann-Whitney U test with tied ranks, Z = -1.74, p =.08), but was significantly different between swarm-unpaired and swarm-paired males in one of the three paired comparisons (Mann-Whitney test with tied ranks, Z = -2.84, p =.0045; Figure 1). Wings were longer in swarm-paired males than in swarm-unpaired ones (mean±SE = 5.04±0.017 versus 4.98±0.010 mm). Larger males mated more successfully in swarms where large males aggregated.
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The mean unsigned values of right-left wing length difference in each sample ranged from 0.019 to 0.028 mm. Across all of the samples, right-left wing length difference ranged from 0.187 mm to 0.000 mm (Figure 2). Right-left difference was not significantly different among any of each three samples of ground-unpaired, swarm-unpaired, ground-paired, and swarm-paired males (Kruskal-Wallis test with tied ranks, H = 3.63, p =.16; H = 0.38, p =.83; H = 0.87, p =.65; H = 2.17, p =.34, respectively). Consequently, each set of three samples were pooled. Comparisons of the pooled samples revealed no significant difference between ground- and swarm-unpaired and between unpaired and paired males from both ground- and swarm-mating (Mann Whitney U test with tied ranks, Z = -1.08, p =.28; Z = -0.69, p =.49; Z = -0.20, p =.84, respectively). Thus, the level of wing asymmetry did not indicate successful males in mating in any of the tactics.
Right-left wing length difference was not uniform against the wing length classes (Figure 3). The linear regression of the difference on wing length was not significant (y = 0.0441-0.0046x, r =.16, F1,8 = 0.20, p >.05). Because the data points for wing length classes of 4.4 and 5.4 mm evidently diverged from the other points, probably due to small sample sizes (Figure 3), they were omitted and the regression was repeated. The quadratic regression was then significant (y = 1.289-0.510x + 0.051x2, r =.90, F2,6 = 12.29, p =.008), suggesting that there was a U-shaped relationship between the right-left difference in wing length and the wing length itself.
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Wing asymmetry represented as right-left wing length difference was
normally distributed and did not deviate from a mean value of 0 in five of six
samples of paired males, indicating they demonstrated FA
(Table 1). However, this was
observed only two of six samples of unpaired males
(Table 1). In the samples
without normality, values of kurtosis were so high relative to sample sizes
that these distributions were leptokurtic
(Table 1), suggesting that they
may have included extremely asymmetric individuals. Statistical tests for
detecting outliers (Sokal and Rolf,
1995) revealed the presence of outliers in five of six samples of
unpaired males and in one sample of paired males
(Figure 2), although the
proportion of outliers did not differ significantly between unpaired and
paired males (Wilcoxon paired-sample test, Z = -0.94, p
=.35). Because measurement error was quite small compared with wing length
difference (see Methods), these outliers were unlikely to be negligible as
measurement errors. Removal of these outliers gave normality to one sample of
ground-unpaired males (Table
1), indicating that they were one of the causes of non-normality
in wing asymmetry among unpaired males. Therefore, these results suggested
that extremely wing-length asymmetric males may have been excluded from
mating.
In a test for zero-mean, two samples of swarm-unpaired males had mean values significantly different from zero (Table 1). They were large samples (n = 181 and 201), and the mean values deviated from zero toward the negative side (left wing > right wing). This may suggest directional asymmetry in wing length.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Previous studies that have described the swarming and ground-mating tactics of T. akamusi have found no morphological, physiological correlate with which to discriminate between males using each tactic. These tactics are seen at different times on the same day. As emergence occurs mostly just after the sunset, dependence of tactics on diurnal timing of emergence is unlikely to occur. In addition, both tactics are observed over the emergence period of about 1 month, so seasonal timing of emergence seems not crucial for the tactics. The results of this study show that large males typically adopt the swarming tactic.
The advantage of large size seems to be a general trend in swarm-mating
insects (e.g., Thornhill,
1980; Yuval,
1993). Large size may be favored because of higher stamina
(Neems et al., 1992,
1998), active female choice,
or increased fighting ability. During the present study, pairs of grappling
males were often seen to fall from the swarm, suggesting that male fighting
may be important. I observed that swarming males had collisionlike contacts
with each other in swarms. However, the role of size in determining fighting
ability is unknown. Further study is required to distinguish the benefit males
obtain from a larger body size. Although the male pairs could be the result of
mistaking a male for a female (Kon et al.,
1986;
Syrj
mki,
1964; Tokeshi and Reinhardt,
1996), the grappling males did not have those morphological
features such as folded antennal fibrillae and swollen abdomens which cause
males to be mistaken for females in mating on the ground.
Males using the searching tactic on the ground are relatively small. The
trend for small dipteran males not to swarm, but instead to remain in the
vegetation adjacent to a swarm, has previously been reported by McLachlan and
Neems (1989). They suggested
that small males exploit the mate-attracting activities of large males in the
swarm. A difference between their study and the present one is the fact that
males of T. akamusi throughout the size range participate in mating
on the ground. Success of mating as a result of searching on the ground was
independent of size. Given that I relied only on this result, small males
might have had no advantage in either of the mating tactics.
Nonetheless, there is a possible advantage of small males in mating. When males mating on the ground were collected, no swarm was observed. But, when swarming males were collected, a number of males, which may have been small ones, were observed on the ground. Some of them on the ground were searching for females or copulating with them. This observation indicates that, when swarms are formed, small males are staying and enjoying the mating on the ground while large males perform swarm mating. This advantage of small males needs to be studied on the lifetime basis because they are engaged in ground mating in the morning, too.
The relationship between trait size and asymmetry has been suggested to
indicate whether the trait size is related to the individual's reproductive
quality (Møller and Hoglund,
1991; Møller and
Pomiankowski, 1993a,
b). In T. akamusi,
the relationship between wing size and right-left wing length difference was
flat or U-shaped (Figure 3),
which likely explains why wing asymmetry was not smaller among large
swarm-paired males than swarm-unpaired ones. This relationship means that the
most abundant, medium-sized individuals had slightly less asymmetry than the
smaller and larger males. The curve may suggest that wing size is subject to
stabilizing selection pressure
(Møller, 1993;
Møller and Pomiankowski,
1993a). Small and large individuals off the optimum medium size
are supposed to have higher asymmetry as a result of failure in controlling
bilateral size development. There is, however, selection for large size by
swarm mating, and there might be selection for small size by search mating on
the ground. If the assumption of stabilizing selection holds, what is the
stabilizing selection working against? It should be that derived from
size-associated asymmetry itself, although it was not obvious within the
present study. Or it might be predation pressure acting against large and
small size. Dragon flies prey on swarming midges, and spiders and mantises
prey on midges on the ground (Kon et al.,
1986). Small males could be under stronger predation pressure on
the ground if they are engaged in ground mating for a longer time. Neems et
al. (1998) vigorously revealed
that the lifetime reproductive success of the chironomid C. plumosus
is greatest for males of intermediate size and also for those of the most
frequent size class. In this species, males mate only in swarms, and the
mating success is higher for small males, but fecundity, longevity, and
stamina are better for large males. In the case of T. akamusi,
alternative mating tactics may place counteractive selection pressures on male
size. These pressures should stabilize male body size in combination with
selection pressures to both extremes of male size.
I paid special attention to the non-normality of wing asymmetry. The outlier contributed to the violation of normality of wing asymmetry. Prevailing normality in the wing asymmetry of paired males (Table 1) suggested that individuals with extremely asymmetric wing length (i.e., outliers) were unsuccessful in mating. The presence of extremely asymmetric individuals also means that they are generated in spite of the assumption that wing length is under stabilizing selection pressure. Extremely asymmetric individuals are possibly a result of mutation or developmental abnormalities and should be individuals of low quality. Comparisons between groups of mated and unmated males may mask the presence of such extremely asymmetric individuals, and should be followed by further inspecting individual asymmetries.
If symmetry is selected for by natural selection, asymmetry would be kept within a narrow range. That may be the case in T. akamusi. Further selection based on wing asymmetry does not appear to occur among males participating in mating. However, it was not only the outliers that contributed to the leptokurtic distributions of wing asymmetry of male midges. Such a distribution shows a higher concentration of individuals near the mean, indicating that individuals with very low asymmetry are superdominant. Whether individual differences within the narrow range of asymmetry are related with an individual's mating success or not needs further study.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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I thank Y. Tsubaki for helpful comments on the present study and T. Iwakuma, Y. Sugaya, and R. Ueno for providing information on the biology of T. akamusi. I am also grateful to S. Plaistow for reading the manuscript and giving valuable comments. This study was partly financed by a grant from the Global Environment Research Program, Japan Environmental Agency, no. F-1, and a grant from the Japanese Ministry of Education, Science and Culture, no. 08458168.
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