cr> 1992 Birkhauser. Verlag, Base1. Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters. Anders Pape Moller.
J. evol.
Biol.
5: 691-699
(1992)
1010~061X/92/04691-09s cr> 1992 Birkhauser
1.50+0.20/O Verlag, Base1
Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters Anders
Pape Moller
Department
of Zoology,
Key words: Fluctuating bursa; sexual selection
Uppsala
University,
asymmetry; Hirundo
Box
561, S-751 rustica;
22 Uppsala,
Sweden
ornaments; Ornithonyssus
Abstract The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress(Parsons 1990). Parasites and diseasesare one kind of environmental stresswhich most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessmentof phenotypic quality and thus in sexual selection. 691
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Mdler
Introduction Many secondary sexual characters are extremely exaggerated versions of ordinary traits and they may therefore be close to their limits of production and maintenance. I thus expect that ornaments demonstrate signs of costs more often than ordinary morphological traits. A potential measure of the cost of bilaterally symmetrical ornaments is their degree of fluctuating asymmetry (Merller, 1990a), which occurs when symmetry is the normal state and there is no tendency for the trait value on one side of the body to be larger than that on the other (Van Valen, 1962; Palmer and Strobeck, 1986). A number of experimental studies have demonstrated that the most extremely ornamented males are preferred as mates by females (e.g. Andersson, 1982a). These most ornamented individuals also generally show the smallest degree of fluctuating asymmetry in their ornaments, but not in other morphological traits (Mraller 1990a; Moller and Hoglund, 1991). This generalization is consistent with the hypothesis that male quality is reliably revealed by the size of their ornament, as suggestedby several models of intersexual selection (Zahavi, 1975, 1977; Andersson, 1982b, 1986; Hamilton and Zuk, 1982; Kodric-Brown and Brown, 1984). Two major causesof fluctuating asymmetry have been identified. First, a large number of experimental and correlational studieshave demonstrated that the degreeof fluctuating asymmetry in morphological traits is increasedunder regimesof different kinds of environmental stress (review in Parsons, 1990). The stress factors vary from food or nutrient deficiency over organic pollutants and heavy metals to elevated levels of sound in the environment (Parsons, 1990). This has important implications for sexual selection and honesty in signalling by means of ornaments becausethe unpredictability of the environment will set upper limits to the expression of morphological traits, particularly exaggerated ones like ornaments (Moller, 1990a). Males will therefore be prevented from cheating by developing ornaments of a size surpassing their quality, because this would be reflected in an increased degree of fluctuating asymmetry in their secondary sexual traits. The second factor, which affects the degree of fluctuating asymmetry, is the heterozygosity of the individual (Palmer and Strobeck, 1986; Parsons, 1990). Heterozygotes generally show much lessfluctuating asymmetry than homozygotes, and this has been demonstrated by higher degreesof asymmetry among individuals at the tails of the phenotypic distributions (which are likely to be the recessiveand dominant homozygotes, respectively), a higher degree of asymmetry in inbred lines, and a higher degree of fluctuating asymmetry among homozygotes as compared to heterozygotes, particularly when these individuals develop in new environments. There could be at least two different reasons for the increased degree of fluctuating asymmetry among homozygotes. (i) Heterozygotes generally show a better ability to grow, reproduce and survive because of the well-known heterozygote advantage (Mitton and Grant, 1984). (ii) The ability of individual hosts to cope with parasites (which include both micro- and macro-parasites) is closely related to the quality of their parasite resistance, which for example includes inherited and acquired immune responses.A large body of evidence suggeststhat heterozygotes produce a more
Parasites
and fluctuating
asymmetry
693
efficient immune defence and generally are more resistant to parasites than are homozygotes (Wakelin and Blackwell, 1988). For example, the large variability in the major histocompatibility complex is closely associated with heterozygosity (Potts and Wakeland, 1990). Parasites have also been suggested to play an important role in sexual selection, either because of the direct fitness effects of parasites through mate choice or by the effects of parasites on the expression of ornaments, but not of other traits, and thereby the indirect expression of host resistance to parasites (Hamilton and Zuk 1982; Read, 1989; Msller, 1990b). The effect of parasites on the extent of fluctuating asymmetry has never been investigated experimentally, although it has been known for long that some kinds of parasites can have severe effects on the appearance of their hosts. I report such a study based on the manipulation of the abundance of the haematophagous tropical fowl mite Ornithonyssys bursa and its effect on the expression of the tail ornaments of its swallow Hirundo rustica host. This host species is particularly suitable for such a study because feather traits are regrown once every year during the annual moult. I attempted to test the following two questions experimentally: (i) Do parasites affect the degree of fluctuating asymmetry of host ornaments more than other morphological traits in the same individuals or than homologous traits in the non-ornamented females?This prediction arisesfrom the fact that ornaments generally have a larger degree of asymmetry than other morphological traits and than homologous traits in females (Moller and Hoglund, 1991). (ii) Do the least ornamented host individuals show the largest degree of asymmetry? If ornament size reliably reflects the quality of individuals, the most ornamented individuals should be better able to cope with stress and for that reason develop symmetrical secondary sexual characters (Moller, 1990a).
Methods I tested whether the tropical fowl mite affected the degree of fluctuating asymmetry in their host by manipulating the mite loads of newly built first clutch swallow nests during the 1988 breeding season at my study site at Kraghede (57”12’ N, 1O”OO’E), Denmark. A detailed description of the study site and the swallow population is given in Moller (1990~). Each nest was randomly assignedto one of the following treatments during the egg laying period; (i) ca. 50 mites were added to the nest; (ii) the nest was sprayed with a 0.46% pyrethrin solution; or (iii) the nest was kept as a control and only visited for a similar amount of time as the nests with treatments (i) and (ii). This manipulation considerably changed the number of haematophagous mites (the largest numbers in nest with mites added, the smallest numbers in sprayed nests, and intermediate numbers in control nests) both in first and second clutch nests, despite the fact that most swallows built a new nest for the second clutch, if the first nest was infested with mites (see Moller, 1990~for details). All the swallows were captured either in mist nets or in sweep nets early during the breeding season and provided with an individually numbered aluminium ring
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Mdler
and a combination of colours on their white ventral sides. I took several standard morphological measurements following capture, but only the following feather measurements are used in the present analysis; tail length (mm) which is the length of each of the two outermost elongated tail feathers; shortest tail length (mm) which is the length of the two shortest central tail feathers; and wing length (mm) which is the length of the left and the right wing using the flattened wing method (Svensson, 1984). The swallows were subsequently assigned to nests by making daily observations throughout the breeding season. Adult swallows return to their previous breeding sites in subsequent years, if they are still alive. A total of 204 out of 208 survivors during the years 198441990 bred in the same site in subsequent years, and the remaining birds moved a maximum distance of 300 m. I was therefore able to capture most of the survivors from the 1988 experiment during the 1989 breeding season. The birds were then measured again using the same methods as described above. I calculated asymmetry for each trait and individual by subtracting the left from the right trait value. These absolute values of asymmetry showed the characteristics of fluctuating asymmetry; most individuals were symmetrical and there was no tendency for the values on one side of the body to be larger than those on the other as evidenced from their normal distribution (p > 0.20, Kolmogorov-Smirnov onesample tests). I therefore transformed the values of asymmetry to their numerical value. The prediction that the parasite treatment should affect the degree of fluctuating asymmetry in the tail ornaments, but not in the other morphological traits, was tested using a one-factor repeated measures ANOVA with parasite treatment and sex as the factors and asymmetry of the three feather traits as the repeated measure. The effect of the size of the tail ornament on the degree of asymmetry was determined using tail length as a covariate in the repeated measures ANOVA.
Results and discussion All three feather characters showed fluctuating asymmetry as revealed by the normal distributions of left minus right trait values and the tendency for most individuals to be symmetrical. The extent of fluctuating asymmetry was considerably larger in male than in female tail length (Table 1), or than in the other feather traits in both sexes (F > 40.72, p < 0.0001). This is also consistent with previous studies demonstrating that absolute asymmetry in ornaments is considerably larger than in other feather traits (Moller, 1990a; Moller and Hoglund, 1991). The effect of the experimental manipulation of mite loads of first clutch nests on the degree of asymmetry in the subsequent year varied between traits and sexes (Fig. 1). The degree of asymmetry for tail length differed significantly between treatments (F = 5.70, d.f. = 2, 114, p = 0.0044): Individuals having nests with increased levels of parasites were more asymmetrical in their tails than were controls which were more asymmetrical than individual males having nests with reduced levels of parasites (Scheffe’s test, p < 0.05; Fig. 1). There was also a significant sex
Parasites
and fluctuating
Table 1. Absolute size and degree swallows.Values are means (SE.). Character Wing length Tail length Short tail length Wing asymmetry Tail asymmetry Short tail asymmetry N
695
asymmetry of fluctuating
Males 126.19 105.34 44.17 0.56 2.49 0.51 59
(0.34) (1.27) (0.26) (0.09) (0.29) (0.10)
asymmetry
(mm)
Females 124.74 89.15 44.56 0.43 0.79 0.54 60
(0.38) (0.86) (0.27) (0.08) (0.12) (0.09)
of feather
traits
in male and female
F
P
8.09 112.12 2.06 1.17 29.47 0.06
0.0053 0.0001 0.043 0.28 0.000 1 0.80
effect (F = 30.63, d.f. = 1, 114,~ < 0.0001): Males showed a marked effect of the experimental treatment on the degree of fluctuating asymmetry, whereas this was not the case for females (Fig. 1). The interaction between sex and parasite treatment was statistically significant (F = 3.54, d.f. = 2, 114, p = 0.032). The difference between sexes was largest for the mites treatment, intermediate for the controls and smallest for the group with sprayed nests (Fig. 1). I tested whether ornaments were more susceptible to the effects of parasites than other feather traits. The degree of asymmetry of the short tail length and wing length of males were both unaffected by the experimental treatment (Fig. 1; short tail length: F = 0.30, d.f. = 2, 114, p = 0.74; wing length: F = 0.75, df. = 2, 114, p = 0.48). There was no sex difference in the effect of the experiment on asymmetry in shortest tail feathers and wings (Fig. 1; short tail length: F = 0.06, df = 1, 114, p = 0.81; wing length: F = 1.13, d.f. = 1, 114,~ = 0.29). The degree of fluctuating asymmetry in the length of the short tail and the wing was therefore not affected by the experimentally manipulated loads of parasites in either sex. A repeated measures ANOVA revealed that there were significant effects of parasite treatment (F = 4.21, d.f. = 2, 117, p = 0.017) character (the repeated measure) (F = 35.43, d.f. = 2, 234, p
