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Small Males Are More Symmetrical: Mating Success in the Midge C~Ironomus Phmosus L

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Small Males Are More Symmetrical: Mating Success in the Midge C~Ironomus Phmosus L him. Behav., 1995, 50, 841-846 Small males are more symmetrical: mating success in the midge C~ironomus phmosus L. (Diptera: Chironomidae) ATHOL McLACHLAN & MICHAEL CANT Department of Agriculture and Biological Sciences, The University of Newcastle upon Tyne (Received 9 December 1993; initial acceptance IO February 1994; final acceptance 24 January 199.5; MS. number: 4542) Abstract. Male Chironomus plumosus most successful at acquiring mates showed lower levels of fluctuating asymmetry in length of wing than their rivals. These males were not of the most common size, but were the smallest in the population. These results are consistent with the prediction that where there is directional selection for small individuals, fluctuating asymmetry will be positively correlated with size. However, for a speciesthat mates on the wing, selection may act upon symmetry per se rather than body size. Uncoupling the effects of size from those of asymmetry suggested that fluctuating asymmetrymight, on its own, account for the observed mating successof C. plumosus. It is suggested that the successof the more symmetrical males is due to their improved acrobatic ability. Chironomus plumosusprovides an example of the importance of fluctuating asymmetry in male characters that are not purely ornamental and these results are therefore more readily interpreted in terms of natural rather than sexual selection. 8 1995 The Association for the Study of Animal Behaviour The ability of a genome to buffer errors in female barn swallows, Hirundo rustica, use the embryogenesisis seen in differences between the size and symmetry of sexually selected male tail right and left sides of traits that are ideally bi- feathers as an estimate of genetic health. Alterna- laterally symmetrical. The degree of this fluctuat- tively, low fluctuating asymmetry in functional ing asymmetry is increased by environmental characters may afford an advantage in intra- stressduring development and has repeatedly sexual competition among males in the absence of been shown to be negatively correlated with fit- epigamic selection, as the result of natural selec- nesscharacters such as longevity, growth rate, tion for aerodynamic performance, for example fecundity and heterozygosity (Mitton & Grant (Msller 1991; Balmford et al. 1993a; Thomas 1984; Palmer & Strobeck 1986; Parsons 1990). 1993). Fluctuating asymmetry is a heritable trait in many On purely Newtonian grounds, size per se is animals(Van Valen 1962; Thornhill & Sauer 1992; expected also to affect aerodynamics. Small flying Watson & Thornhill 1994) and thus may be a devices, whether animal or machine, have a measureof overall fitness. smaller turning moment than larger ones. This Fluctuating asymmetry is also associated with effect is also subject to natural selection and variation in male mating success: individuals can have independent consequences for mating with relatively low levels of fluctuating asymmetry success (reviewed by Alexander et al. 1978 and are often found to achieve a greater proportion specifically for chironomids by A. J. McLachlan & of matings (e.g. Thornhill 1992a, b; Liggett et al. R. M. Neems, unpublished data). There are thus 1993; Radesgter & Halldbrsdbttir 1993). This at least two characters that may be important in might be expected since males with low levels of the mating successof midges such as C. plumosus: fluctuating asymmetry are likely to be of superior fluctuating asymmetry and size. overall fitness. Msller (1990) suggested that In C. plumosus the relationship between size and mating successis an unusual one. There is a Correspondence: A. McLachlan, Department of tendency to think of large size as the universal Agriculture and Biological Sciences, The University of determinant of mating success in the male (see Newcastle upon Tyne, Newcastle upon Tyne NE1 7RU, U.K. M. Cant is now at the Department of Zoology, Greenwood & Adams 1987 for a review). In University of Cambridge, Downing Street, Cambridge C. plumosus, however, small males gain a dispro- CB2 3EJ, U.K. portionately high number of matings in aerial 0003-3472/95/090841+06 $12.00/O in 1995 The Association for the Study of Animal Behaviour 841 842 Animal Behaviour, 50, 3 swarms which are visited by females for copu- variables such as wing length and asymmetry. lation (see McLachlan & Neems, in press, for a fluctuating asymmetry was calculated as the review). Patterns of fluctuating asymmetry in absolute difference between right and left wine traits under stabilizing selection often vary with lengths to the nearest 0.05 mm. Where slopesafp trait magnitude in a U-shaped manner. This is not involved, as in comparing means, we adopt because extreme phenotypes show less develop- relative fluctuating asymmetry as the measureof mental stability than those close to the mean of symmetry. Relative fluctuating asymmetry was the population (SoulC & Cuzin-Roudy 1982). calculated as absolute fluctuating asymmetry/wine Here we measure the relationship between trait length. This measure is suitable for application size and fluctuating asymmetry in a specieswhere to our data where many individuals show no it is known that there are advantages to small size. measurable difference between wings. Wings were We have two aims. First, we test the hypothesis measured from the distal edge of the anal lobe to that there is detectable fluctuating asymmetry in the wing-tip at 40 x under a dissecting micro.j male C plumosus and that there is variability in scope fitted with a calibrated eye-piece. We I the degree of fluctuating asymmetry between determined the repeatability of measurements by males. Second, we set out to separate the effects of measuring a single wing 100 times. The variance size and of fluctuating asymmetry on the mating of this within-wing sample was compared to the success of C. plumosus and examine the impli- variance of the difference between left and rigL cations for the evolution of the mating system in wings in our sample of male flies from the swarm this species. For the purposes of this test, data from the first 100 flies measured wei% used. A variance ratio test on log,,X transformed measurements shows thal METHODS within-wing variance is significantly smaller than between-wing variance (FIg8 = 55.8, N, = N,= 100, We measured fluctuating asymmetry as the differ- BO.001). This means that measurement error is ence between the two wings and body size as mean unlikely to affect our ability to detect asymmetry wing length. The latter is an appropriate measure between wings. To avoid individual bias, all wings of body size (1) because wing length is strongly were measured by one of us (M.C.). The single correlated with other measures of size such as dry exception was a subset of 25 male flies which we weight in chironomids (McLachlan 1986) and (2) both measured as a second check against bias. In because mean wing length and the difference this test the number of asymmetrical individuals between wings are statistically independent vari- found was identical in both cases. ables. Wing lengths were measured in 224 males The majority of individuals had no measurable collected by net from mating swarms. We also asymmetry and detectable differences were always measured 135 male-female pairs, captured either one or two of the smallest scale divisions, so while they were mating. Samples were taken in we followed the advice of Sullivan et al. (1993) the evenings between April and June 1992 at in grouping individuals into size classes.An inter. Washington Wildfowl Park, Northumberland. val of 0.2 mm by mean wing length was chosen Swarms of males form over landmarks each and mean absolute fluctuating asymmetry was evening in order to attract dispersed mates. calculated for each class. The difficulty of using Searching females enter the swarm and leave mean wing length is that a damaged wing is it again after a short period paired with a male. necessarily shorter than the other and a false The pair are poor fliers and settle briefly near average is the consequence. However, we were the swarm (McLachlan & Neems, in press). able to detect damage readily and so the use of Net sweeps through such swarms yield mostly mean wing length is acceptable (see Cuthill et al. unpaired males while paired males and their 1993). mates can be captured on the ground near the We used least-square regression analysis to swarm. determine whether a relationship exists between To avoid statistical difficulties associated with absolute fluctuating asymmetry and wing length. the measurement of relative fluctuating asym- To test the slope of the regression against a null metry (Cuthill et al. 1993; Mraller 1993; Sullivan hypothesis of allometry we followed Alatalo et al. et al. 1993), when examining slopes relating two (1988), Fairbairn (1992), Green (1992) and Petrie McLachlan & Cant: Fluctuating asymmetry in midges 843 11992),in using reduced major axis regression (RMA). We tested the significance of departure of the observed slope (bRMA) from allometry with a Studentst-test (Sokal & Rohlf 1981). RMA data werefirst transformed log,,X on both axes. We separated the effects of fluctuating asymme- try and of wing length on mating successby using relative fluctuating asymmetry as a measure of symmetry.We also compared males and females overthe same size range to test hypotheses about the relationship between wing length and absolute tluctuating asymmetry in males. All statistical testswere two tailed and considered significant at alphaof 5%. RESULTS Measurementsof absolute fluctuating asymmetry in males from mating swarms showed no tendency 3.4 4.0 5.0 5,.f 6 for one wing to be longer than the other (142 Wing length class (mm) males showed no difference between right and left measurements,47 had a longer right wing, 35 had Figure 1. Mean fluctuating asymmetry versus wing length class in unmated male C. p~umosus collected from a longer left wing; sign test binomial: PO.05). swarms.
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