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Sexual selection, viability selection, and developmental stability in the domestic fly Musca domestica.

Sexual selection arises as a result of "the advantages that certain individuals have over others of the same sex and species, in exclusive relation to reproduction" (Darwin 1871). Two processes may give rise to sexual selection, namely competition between individuals of the chosen sex for access to individuals of the choosy sex, and choice of partners by individuals of the choosy sex (Darwin 1871). Choosy females may benefit from their mate choice because of direct or indirect fitness benefits. Direct benefits include parental care and resource provisioning (Hoelzer 1989; Heywood 1989; Grafen 1990; Price et al. 1993), while indirect benefits can arise from arbitrary male attractiveness (Fisher 1930; Lande 1981; Pomiankowski et al. 1991) or viability signalled by a secondary sexual character (Zahavi 1975; Hamilton and Zuk 1982; Kodric-Brown and Brown 1984; Andersson 1986; Heywood 1989; Iwasa et al. 1991).

Developmental stability of morphological characters may be one important target of sexual selection (Moller 1990a; reviews in Moller 1993e; Watson and Thornhill 1994). The reasons for this argument are twofold. First, the level of developmental stability, for example measured in terms of fluctuating asymmetry (FA), reflects the overall ability of individuals to cope with genetic and environmental stress (Palmer and Strobeck 1986; Parsons 1990). Measures of developmental stability will thus reliably reflect the genotypic and phenotypic constitution of potential mates. Second, signals subject to a directional mate preference are developmentally more unstable than characters predominantly subject to stabilizing selection (Moller and Pomiankowski 1993). Characters involved in sexual selection will thus on average be much more variable than other characters, and this variability is the raw material for the two processes of sexual selection. A total of 21 studies has investigated the relationship between developmental stability and sexual selection, and 18 of these found evidence in agreement with the hypothesis that sexual selection should result in a mating advantage for developmentally stable individuals (Moller 1993e and unpubl.). The kinds of benefits accruing to individuals choosing developmentally stable mates could be any of the three major kinds of fitness benefits, i.e., direct benefits, genes for male attractiveness, or genes for viability (Moller 1993e). Direct fitness benefits are less likely in mating systems without any resources or parental care. Preconditions for the good genes process of sexual selection are that (1) there is genetic variance in viability, and (2) phenotypic variance in the character that is the target of selection reliably reflects viability differences.

In this study I report on the association between developmental stability of morphology and sexual selection in Musca domestica (Muscidae, Diptera). The association between viability selection and sexual selection for developmentally stable individuals is also investigated in two different ways. First, measures of developmental stability such as individual FA may reflect overall phenotypic quality, and individuals with high degrees of asymmetry should thus perform less well in a number of different contexts because the inability to cope with one kind of stress also appears to be associated with the inability to cope with others (Hoffmann and Parsons 1989). Stressed individuals of low phenotypic quality are often affected by parasites (Noble and Noble 1976; Cox 1982), and since FA develops in direct response to stress, individuals with high FA may therefore be predicted to be more susceptible to parasitism than individuals with low degrees of asymmetry. This prediction was investigated in two different ways: by comparison of the level of asymmetry of flies that had died from infections by the entomopathogenic fungus Enthomophthora muscae (Zygomycetes, Entomophthorales) with the asymmetry of the nearest neighboring fly that had died for other reasons, and by estimating the likelihood of developing infections by the parasitic fungus for previously uninfected flies differing in their degree of asymmetry. The main cause of mortality during late summer and early autumn in farm populations of domestic flies is fungus infections by E. muscae, and density-dependent infections result in an annual population crash (J. Keiding, pets. comm. 1984). Flies dead for 'other reasons' thus belong to the small proportion of the population that has either not been exposed to fungus spores or is resistant to fungus infections.

Second, if FA is an indication of individual quality, then individuals that fall prey to predators should be relatively more asymmetric than survivors. Predators do not capture all prey items that are pursued, because some potential prey may evade capture, for example, by evasive movements. Since FA directly may affect the performance of individuals by influencing their movements (Moller 1991), the ability to escape predation attempts should be directly related to the degree of morphological symmetry. The test presented here consists of pairwise comparisons of the degree of FA in flies falling prey to the barn swallow Hirundo rustica (Hirundinidae, Aves), which is a common predator of flying insects, and in surviving flies captured by an observer in the same site as prey captured by the predator.

MATERIALS AND METHODS

Study Organisms

Musca domestica is a generalist dipteran insect closely associated with human habitation. Eggs are laid in fermenting debris where the larvae develop, pupate and eclose within approximately two weeks depending on the temperature. Females mate multiply during the fertilization of a single batch of eggs. Males compete for access to females, and male interference during copulations is common (Colwell and Shorey 1975). Fecundity is size-related with large females laying more eggs (Lobanov 1977). Morphological characters like the length of wings and tibia are heritable and have considerable amounts of additive genetic variance (Bryant 1977; Bryant and Turner 1978).

Entomophthora muscae infects the adult domestic fly M. domestica (King and Humber 1981; Samson et al. 1988). Germ tubes of E. muscae most frequently enter into the abdomen of its host (Brobyn and Wilding 1983), where they expand to a bladder-like hypha from which hyphal bodies develop, causing death of the host within less than one week after infection (Brobyn and Wilding 1983). Approximately 12 h after death conidiophores emerge from intersegmental membranes. Flies often die at exposed sites and stick in an upright position to the substratum by their proboscis and legs (Brobyn and Wilding 1983). Spores are subsequently discharged from primary and secondary (and sometimes tertiary) conidia at a maximum rate 10-12 and 30 h post mortem, respectively (Mullens and Rodriguez 1985). Many flies are infected by spores discharged from conidia, although flies also become infected by contact-transmission. Rates of transmission are positively related to host population density and reach maximum values during warm humid conditions in late summer (Mullens et al. 1987). Lower humidity at other times of the year reduces infection rates. Although increased numbers of infected flies have been shown to increase rates of transmission (Mullens 1985), one direct mechanism appears to be parasite manipulation of host sexual behaviour (Moller 1993a).

The barn swallow Hirundo rustica is an aerially insectivorous passerine bird that captures insects on the wing. Individual prey items are pursued and captured in active flight. The majority of prey during the reproductive season are Diptera, and Muscidae comprise the largest fraction in terms of biomass (Cramp 1985; Glutz von Blotzheim and Bauer 1985).

Study Site

Observations and experiments were done in eight dairy farms at Kraghede (57 [degrees] 12[minutes] N, 10 [degrees] 00[minutes] E), Denmark, during the summers 1992-1993. Fly populations reached peak density during July-August.

Measurement of Flies

All flies measured had intact wings and front legs. Left and right wings and front legs were mounted between two glass slides. Measurements of the length of wings (which as defined in this paper was slightly less than the total length of wings) and tibia were subsequently made under a stereo microscope with a 20x magnification and an accuracy of 0.005 mm ([ILLUSTRATION FOR FIGURE 1 OMITTED] for definitions of measurements). All preparations and measurements were done blindly by a student who did not know the status of flies (whether mated, infected or depredated).

The absolute level of fluctuating asymmetry for individual flies was estimated as the unsigned left-minus-right character value and relative asymmetry was estimated as absolute asymmetry divided by the mean left and right character value (Ludwig 1932; Palmer and Strobeck 1986). The two characters did not demonstrate directional asymmetry since mean signed left-minus-right character values for each of the samples did not deviate significantly from zero (one sample t-tests, P [greater than] 0.05 in all cases). The two characters did not demonstrate anti-symmetry since the frequency distributions of signed left-minus-right character values did not deviate significantly from normal distributions (one-sample Kolmogorov-Smirnov tests, P [greater than] 0.05 in all cases).

The two morphological characters and their absolute asymmetries were measured twice on two different days in ten individuals. The repeatability of the two length measurements and their asymmetry was very high and statistically significant (wing length: R = 0.99 (SE = 0.013), F = 159.36, df = 9,10, P [less than] 0.001; tibia length: R = 0.99 (SE = 0.005), F = 78.78, df = 9,10, P [less than] 0.001; absolute wing asymmetry: R = 0.97 (SE = 0.018), F = 74.15, df = 9,10, P [less than] 0.001; absolute tibia asymmetry: R = 0.98 (SE = 0.016), F = 67.40, df = 9,10, P [less than] 0.001 (Falconer 1989; Becker 1984)). This suggests that the measurements were sufficiently precise to allow analyses of the morphological traits and their asymmetries.

Sexual Selection Experiment

Mated and unmated flies were collected from farms in the study area during the period 15 July-15 August 1992. I collected mated flies when a fly mounted and copulated with another fly. An unmated fly next to the copulating pair was also collected simultaneously for comparison. The test thus consisted of a pairwise comparison of the morphological measurements of a mated and an unmated fly from the same site and time. Even though currently unmated flies may mate at other times, this pairwise comparison procedure provides an unbiased estimate of the morphology of flies in relation to mating frequency. The reason is that any morphological difference associated with mating frequency should result in a morphological difference between flies that are currently mating and those that are not mating. A total of 50 pairwise collections was made for each sex.

Results from these pairwise comparisons may partly be confounded by flies differing in age or other respects. Therefore, the role of sexual selection was investigated further in two series of experiments in July 1993. Virgin flies aged 510 days originating from pupae collected from farms were placed in glass vials either as two females and one male (two females experiment) or two males and one female (two males experiment). The glass vials were cylindrical with a diameter of 50 mm and a height of 75 mm. Only one experiment was performed on flies originating from a single site. The first female (two females experiment) or male (two males experiment) to copulate was marked with white correction fluid, and its morphology was compared in a pairwise comparison with that of the individual not involved in the copulation. A total of 25 replicates was made for each sex, in total 50 replicates.

Fungus Infection Experiment

The morphology of infected and uninfected flies was compared based on collection of dead flies in July 1992. Flies were collected pairwise by identification of individuals dead from infection with the entomopathogenic fungus, as evidenced from the white bands of conidiophores extending from the intersegmental bands of the abdomen, and the nearest neighbouring dead fly without clear signs of conidiophores. The test thus consisted of pairwise comparisons of the morphology of these pairs of flies. A total of 25 pairs was collected of each sex.

The relationship between developmental stability and susceptibility to the entomopathogenic fungus was tested in experiments in July 1993. The dorsal side of the abdomen of two virgin flies of the same sex originating from pupae that was collected from farms was allowed to touch one band of conidiophores of an infected dead fly and each was then placed in a glass vial on a diet of milk powder, sugar and water. Each replicate was performed on flies originating from a single site. Infection was determined by recording whether or not flies had died and developed conidiophores one week after touching the infected fly. A total of 75 replicates, in which 49 males and 40 females became infected, was made for each sex. I investigated data from pairs of flies in which one died and the other did not (pairs in which both flies or neither became infected were therefore eliminated), and the test thus consisted of pairwise comparisons of the morphology of infected and uninfected individuals.

Predation on Flies

Foraging barn swallows feeding nestlings were provided with different combinations of color markings on their bellies for identification. I followed barn swallows foraging near barns and noted when flies were captured. I subsequently collected flies with a sweep net in the same site, and the flies fed to barn swallow nestlings were collected by providing nestlings with neck collars which prevented them from swallowing the food boluses. The morphology of one randomly chosen fly from the food bolus was compared with that of one randomly chosen fly of the same sex from the field sample. In order to avoid pseudo-replication, only a single sample originated from each individual barn swallow. The test consisted of pairwise comparisons of the morphology of flies captured by barn swallows and flies subsequently captured with a sweep net in the same site. Although it may seem unlikely that all flies that were classified as survivors actually evaded a capture attempt by the birds, the comparison between flies that were captured and those that were not equals a comparison between depredated flies and flies belonging to the population. Although current survivors may fall prey to barn swallows at other times, the pairwise comparison procedure provides an unbiased estimate of fly morphology in relation to predation status. Morphological differences associated with predation rate should give rise to morphological differences between flies that just have fallen prey to birds and those that have survived.

Insects captured by barn swallows are collected in a small bolus containing saliva, on average 15 insects per bolus (Moller 1994b). Insect wings and other morphological traits of individuals captured by barn swallows are almost always intact, and measurements can easily be made following extraction from the bolus with the help of a pin and a pair of pincers. A total of 25 pairwise replicates was made for each sex.

Statistical Procedures

The statistical tests consist of pairwise comparisons because the morphology of focal flies was compared with nearest neighbors differing in mating, infection, or predation status. Most comparisons were non-parametric Wilcoxon matched-pairs signed-ranks tests (Siegel and Castellan 1988).

Probability values were adjusted for the repeated statistical tests (a total of six tests were made on each data set) using a sequential Bonferroni correction (Rice 1989), and the significance level was set to 0.05. Values given are means (SE).
TABLE 1. Morphology of free-living domestic flies in relation to
mating status. Values are means (SE). Z-values are from Wilcoxon
matched-pairs signed ranks tests.


Character                     Unmated           Mated          z


Males


Wing length (mm)            8.65(0.14)       9.11(0.14)      1.83
Tibia length (mm)           3.02(0.10)       3.05(0.07)      0.41
Absolute wing FA (mm)       0.183(0.034)     0.069(0.021)
2.41(*)
Absolute tibia FA (mm)      0.083(0.027)     0.046(0.022)    1.06
Relative wing FA            0.021(0.004)     0.008(0.002)
2.54(*)
Relative tibia FA           0.027(0.009)     0.015(0.007)    0.92
N                                50             50


Females


Wing length (mm)            9.20(0.30)       9.14(0.15)      0.09
Tibia length (mm)           3.12(0.05)       3.17(0.03)      0.94
Absolute wing FA (mm)       0.148(0.029)     0.027(0.012)
3.36(*)
Absolute tibia FA (mm)      0.059(0.019)     0.047(0.013)    0.64
Relative wing FA            0.017(0.004)     0.003(0.001)
3.44(*)
Relative tibia FA           0.019(0.006)     0.015(0.004)    0.90
N                                50               50


* Statistically significant at P [less than] 0.05.


RESULTS

Phenotypic Correlations

The lengths of the two morphological characters were weakly positively correlated with Kendall rank correlation coefficients ranging from -0.03 to 0.28, n = 10 samples (in Tables 1-5), and nine of ten coefficients were positive (deviating significantly from equally many positive and negative coefficients, sign test, P = 0.022). The two absolute measures of fluctuating asymmetry were weakly positively correlated with Kendall rank correlation coefficients ranging from -0.11 to 0.37, n = 10 samples, and nine of ten correlation coefficients were positive (which deviates significantly from many equally positive and negative coefficients, sign test, P = 0.022). This result suggests that the two kinds of fluctuating asymmetry may reflect the same phenomenon.
TABLE 2. Morphology of domestic flies in relation to mating status
in sexual selection experiments. Values are means (SE). Z-values
are
from Wilcoxon matched-pairs signed ranks tests.


Character                     Unmated           Mated          z


Males


Wing length (mm)            8.88(0.13)       8.92(0.08)      0.23
Tibia length (mm)           3.01(0.07)       2.97(0.08)      0.67
Absolute wing FA (mm)       0.124(0.023)     0.032(0.009)
3.59(*)
Absolute tibia FA (mm)      0.064(0.017)     0.024(0.008)
2.66(*)
Relative wing FA            0.014(0.002)     0.004(0.001)
3.69(*)
Relative tibia FA           0.021(0.002)     0.008(0.001)
2.69(*)
N                                25               25


Females


Wing length (mm)            9.15(0.15)       9.10(0.16)      0.30
Tibia length (mm)           3.16(0.03)       3.14(0.03)      0.27
Absolute wing FA (mm)       0.072(0.018)     0.025(0.008)
2.50(*)
Absolute tibia FA (mm)      0.051(0.011)     0.040(0.010)    1.17
Relative wing FA            0.008(0.002)     0.003(0.001)
3.27(*)
Relative tibia FA           0.016(0.003)     0.013(0.002)    1.23
N                                25               25


* Statistically significant at P [less than] 0.05.


Fluctuating asymmetry was weakly negatively related to character size for both tibia and wings of both sexes (10 samples of each sex: males: tibia: standardized regression coefficients ranging from -0.05 to -0.24, mean (SE) = -0.145 (0.03), t = 4.83, df = 9, P [less than] 0.05; wings: standardized regression coefficients ranging from -0.04 to -0.21, mean (SE) = -0.152 (0.03), t = 5.07, df: 9, P [less than] 0.05; females: tibia: standardized regression coefficients ranging from -0.03 to -0.23, mean (SE) = -0.140 (0.02), t = 6.82, df = 9, P [less than] 0.05; wings: standardized regression coefficients ranging from -0.02 to -0.12, mean (SE) = -0.064 (0.01), t = 5.33, df = 9, P [less than] 0.05). Larger individuals thus tended to be more symmetrical than smaller individuals.

Sexual Selection and Asymmetry

The morphology of mated flies was compared with that of nonmating, nearest neighboring flies from a free-living population. The results differed between the sexes. Mated male flies had slightly longer wings than unmated males while tibia length did not differ with respect to mating status (Table 1). Both wing and tibia asymmetry was larger in unmated than in mated males, but the difference was only statistically significant for wing asymmetry (Table 1). Wing asymmetry was more than twice as large in unmated as in mated flies, and tibia asymmetry differed by 80%. Female mating success was unrelated to the length of wings and tibia, but wing FA differed between mated and unmated females (Table 1). Unmated females had more than five times as large wing asymmetry as mated females. There were small, nonsignificant differences in tibia asymmetry.

Sexual selection experiments with two individuals of one sex and one individual of the other confirmed these observations of a relationship between developmental stability and mating status. When two males were presented to a single female in an experiment, the male that first mated had more symmetric tibia and wings than the unmated male (Table 2). This was not due to an absence of courtship behavior by the unmated male, because the unmated male courted the female in 72% of the 25 replicates. The reverse experiment with two females and one male revealed a statistically significant difference in wing asymmetry, but no tibia asymmetry difference between females of different mating status. The male courted even the female that was not mated first in 52% of the 25 replicates.

Parasite Infection and Asymmetry

The morphology of flies infected by the entomopathogenic fungus was compared with that of the nearest dead uninfected flies. The only characters that differed with respect to infection status was male wing length and female wing asymmetry (Table 3). Wing asymmetry of infected flies was almost 60% larger than among uninfected flies (Table 3).

Experimental application of fungus spores resulted in infection of flies in 63.3% of the males (n = 75) and 53.3 % of the females (n = 75). Pairwise comparison of the morphology of infected and uninfected flies revealed that both infected male and female flies were significantly more asymmetric in their wings (Table 4). These results thus confirmed the relationship between wing asymmetry and infection status in free-living flies.
TABLE 3. Morphology of free-living domestic flies in relation to
infection status. Values are means (SE). Z-values are from Wilcoxon
matched-pairs signed ranks test.


Character                    Uninfected        Infected        z


Males


Wing length (mm)            9.53(0.13)       9.64(0.09)
3.90(*)
Tibia length (mm)           3.10(0.02)       3.07(0.02)      0.09
Absolute wing FA (mm)       0.052(0.012)     0.074(0.016)    2.04
Absolute tibia FA (mm)      0.044(0.010)     0.056(0.014)    0.69
Relative wing FA            0.033(0.007)     0.046(0.010)    2.04
Relative tibia FA           0.027(0.006)     0.035(0.009)    0.69
N                                25               25


Females


Wing length (mm)            9.27(0.15)       9.99(0.11)      0.65
Tibia length (mm)           3.09(0.05)       3.10(0.03)      0.63
Absolute wing FA (mm)       0.052(0.013)     0.086(0.016)
2.50(*)
Absolute tibia FA (mm)      0.036(0.013)     0.028(0.009)    0.51
Relative wing FA            0.033(0.008)     0.054(0.010)
2.50(*)
Relative tibia FA           0.017(0.006)     0.022(0.008)    0.51
N                                25               25


* Statistically significant at P [less than] 0.05.


Predation and Asymmetry

The morphology of flies captured by barn swallows and fed to their offspring was compared with the morphology of survivors in a pairwise fashion. Flies captured by barn swallows had more asymmetric tibia and particularly more asymmetric wings than flies surviving capture attempts (Table 5).

DISCUSSION

Developmental Stability and Sexual Selection

Developmental stability may play an important role in sexual selection because it represents a general health certificate of an individual under the given environmental conditions (Moller 1990a, 1992a,b; 1993b,c,d,e; 1994a; Moller and Pomiankowski 1993; Thornhill 1992a,b,c; Thornhill and Sauer 1992; Watson and Thornhill 1994). Although the great majority of studies of developmental stability and sexual selection documented a positive relationship between fluctuating asymmetry and mating success, a couple of studies were unable to do so (reviews in Moller 1993e; Watson and Thornhill 1994). The present study demonstrated a selective advantage for individuals with symmetric wings in terms of sexual selection (Tables 1-2). A similar relationship between FA and sexual selection has been recorded in Scatophaga stercoraria, probably because symmetric males were more successful in male-male competition (Liggett et al. 1993). Both female choice and male-male competition appeared to play an important role in some studies of the relationship between developmental stability and sexual selection (Radesater and Halldorsdottir 1993), while either female choice or male-male competition dominated in others (Moller 1992a, 1993d; Liggett et al. 1993).
TABLE 4. Morphology of domestic flies in relations to infection
status in infection experiments. Values are means (SE). Z-values
are
from Wilcoxon matched-pairs signed ranks tests.


Character                    Uninfected        Infected        z


Males


Wing length (mm)            9.56(0.11)       9.57(0.10)      0.66
Tibia length (mm)           3.07(0.04)       3.09(0.05)      0.70
Absolute wing FA (mm)       0.050(0.014)     0.179(0.033)
3.76(*)
Absolute tibia FA (mm)      0.069(0.012)     0.125(0.028)    1.38
Relative wing FA            0.006(0.002)     0.021(0.004)
3.07(*)
Relative tibia FA           0.023(0.004)     0.043(0.011)    0.84
N                                49               49


Females


Wing length (mm)            9.80(0.09)       9.87(0.09)      0.21
Tibia length (mm)           3.18(0.03)       3.13(0.02)      1.47
Absolute wing FA (mm)       0.072(0.016)     0.192(0.021)
3.84(*)
Absolute tibia FA (mm)      0.048(0.014)     0.080(0.019)    1.21
Relative wing FA            0.008(0.002)     0.022(0.002)
3.99(*)
Relative tibia FA           0.015(0.004)     0.025(0.006)    1.43
N                                40               40


* Statistically significant at P [less than] 0.05.


Development Stability and Viability

Developmental stability and parasitism should be associated for theoretical reasons. Parasitism is often associated with stress in hosts (Noble and Noble 1976; Cox 1982), and fluctuating asymmetry in morphology is a reliable indicator of the ability to cope with genetic and environmental stress during development (e.g., Parsons 1990). The elevated level of FA in flies dead from the entomopathogenic fungus is thus in accordance with this expectation (Table 3). Parasitism has previously been shown to be associated with developmental stability (Moller 1992c; Polak 1993). Moller (1992c) demonstrated experimentally that the presence of one haematophagous ectoparasite subsequently gave rise to increased FA in a secondary sexual character, but not in two ordinary morphological characters. Therefore, FA in the secondary sexual character directly revealed ability to cope with the parasite. Nematodes infecting Drosophila nigrospiracula larvae appeared to cause increased levels of abdominal bristle asymmetry in adult flies, implicating a causal relationship between nutritional stress during host development and fluctuating asymmetry (Polak 1993). In conclusion, these two studies indicate that large levels of FA develop as a consequence of parasite infections.
TABLE 5. Morphology of free-living domestic flies surviving or not
surviving attacks by barn swallows. Values are means (SE). Z-values
are from Wilcoxon matched-pairs signed ranks tests.


Character                     Survivors      Nonsurvivors      z


Males


Wing length (mm)            8.99(0.12)       9.01(0.07)      0.58
Tibia length (mm)           3.06(0.03)       3.04(0.06)      1.33
Absolute wing FA (mm)       0.044(0.010)     0.188(0.019)
4.83(*)
Absolute tibia FA (mm)      0.048(0.013)     0.112(0.028)    1.66
Relative wing FA            0.005(0.001)     0.021(0.002)
4.50(*)
Relative tibia FA           0.016(0.004)     0.038(0.011)    1.05
N                                25               25


Females


Wing length (mm)            9.32(0.11)       9.20(0.13)      1.32
Tibia length (mm)           3.14(0.02)       3.19(0.02)      1.14
Absolute wing FA (mm)       0.048(0.018)     0.146(0.013)
4.43(*)
Absolute tibia FA (mm)      0.032(0.010)     0.098(0.019)
2.82(*)
Relative wing FA            0.005(0.002)     0.016(0.001)
4.48(*)
Relative tibia FA           0.010(0.003)     0.030(0.006)
2.77(*)
N                                25               25


* Statistically significant at P [less than] 0.05.


Fluctuating asymmetry also may be associated with parasitism because FA directly reveals the susceptibility of hosts to parasite infections. Individuals with high levels of FA may have an increased probability of infection because of their movements or habitat preferences. Reduced general vigor as reflected by elevated levels of FA may result in asymmetric individuals experiencing an increased probability of encountering parasites. This would be the case if asymmetric male flies became infected with the fungus because they particularly were attracted to the corpses of spore-producing conspecifics (Moller 1993a). Dead flies infected with the fungus are sexually attractive to males (Moller 1993a), and asymmetric males may be particularly attracted because of their relatively low mating success (this study). Alternatively, if competitive ability is associated with FA, asymmetric individuals may be more likely to encounter habitats where the risk of contracting parasite infections is high. Both these explanations could account for the association between wing asymmetry and fungus infection in female domestic flies (Table 3). However, these explanations could not account for the result that asymmetric flies indeed were more likely to become infected in the infection experiment (Table 4). Individual flies may develop an asymmetric phenotype because of environmental or genetic stress, and such individuals may also be less able to raise an immune response or in other ways defend themselves against parasites.

The second kind of viability selection associated with developmental stability arose from bird predation. Flies with asymmetric tibia and particularly with asymmetric wings were more often captured by foraging barn swallows than symmetric flies (Table 5). This association between FA and predation is likely to be due to the direct effects of asymmetry on performance. Even small asymmetries in morphological characters used in flight are hypothesized to severely affect flight performance (Norberg 1989; Thomas 1993). This prediction has been verified experimentally by recording flight performance of barn swallows after manipulation of the level of asymmetry in their tail feathers (Moller 1991). Even small degrees of asymmetry in morphological characters associated with the locomotory apparatus are likely to affect performance. The association between FA and predation risk found in flies may therefore be a more general phenomenon.

Developmental stability has in a recent review been found to have a small, but statistically significant heritability, on average 0.27 (SE = 0.08) in 34 studies of 14 different species (Moller and Thornhill, in press). Heritability studies of developmental stability in particular species usually reveal estimates not significantly different from zero, but the power of the statistical tests is generally low because of large standard errors of the estimates and small sample sizes (Moller and Thornhill 1996). The general result that developmental stability has a small, additive genetic component implies that given there is genetic variance for developmental stability in the domestic fly, sexual selection may give rise to indirect fitness benefits in terms of production of developmentally stable offspring.

In conclusion, the association between developmental stability and two kinds of viability selection suggests the sexual selection for more symmetric flies may give rise to indirect fitness benefits in terms of parasite resistance and predator avoidance.

ACKNOWLEDGMENTS

K. Lindstrom kindly made preparations and measurements of all flies. I would like to thank J. T. Manning, L. Simmons, B. G. Svensson, and two anonymous referees for constructive criticism. The study was supported by a grant from the Swedish Natural Science Research Council.

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Date:Apr 1, 1996
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