Lifetime reproductive success in a swarming midge: trade-offs and stabilizing selection for male body size

Behavioral Ecology Vol. 9 No. 3: 279-286 Lifetime reproductive success in a swarming midge: trade-offs and stabilizing selection for male body size Rachel M. Neexns," John Lazarus,1" and Athol J. McLachIanc Body size in male animals has profound effects on fitness; large males are commonly favored by sexual selection. However, if body size is a stable trait, then advantages of large size must be balanced by disadvantages. In males of the midge Chmmomus plumosus we identified the trade-offs that result in stabilizing selection on body size. Trie smallest individuals have the greatest mating advantage in swarms, perhaps due to their greater agility in capturing females. This measure of mating success in the individual's own swarm was corrected to a population-level measure to take account of the positive correlation between body size and swarm size, the relationship between swarm size and mating success, and the distribution of swarm sizes on an evening. The small male advantage is maintained in the population-level measure. In contrast, large males have greater fecundity and, when unfed, live longer and can remain longer in the swarm each evening (due to their greater stamina). Consequently, lifetime reproductive success is greatest for males of intermediate size, and the most successful body-size class closely matches the most frequent class in the wild. This represents, to our knowledge, the first evidence of stabilizing selection on body size in males of an insect species, as measured by tradeoffs in lifetime reproductive success. Key words: body size, Chirorumus plumosus, lifetime reproductive success, mating success, midge, sexual selection, stabilizing selection. [Behav Ekol 9:279-286 (1998)] B ody size is an important determinant of fitness irj animals (e.g., Qutton-Brock, 1988), and in insects large males often enjoy greater mating success (Partridge, 1988; Partridge and Farquhar, 1983; Pitnick, 1991; Thornhill and Alcock, 1983), fecundity (Southwood, 1966), and longevity (Banks and Thompson, 1985; Neems et al., 1990; Partridge and Farquhar, 1983). However, if body size is a stable trait, then some components of lifetime reproductive success (LRS) must favor small size, body size being maintained by stabilizing selection as an optimal compromise between die benefits of large and small size. Small males have greater mating success in some insects, for example (Banks and Thompson, 1985; Neems et aL, 1990). There is evidence for stabilizing selection on body size in female insects, in which larger size increases fecundity but also increases development time (Roff, 1981, Sibry et al., 1991). In male insects, in which size is subject to sexual selection, studies of LRS have often found selection not to be stabilizing (Koenig and Albano, 1987; Partridge, 1988; Santos et al., 1992; Simmons, 1988). Although greatest lifetime mating success has been reported for males of intermediate size in some species (Fincke, 1988; Thompson, 1989), ignorance of the possible effect of male size on fecundity makes the case for stabilizing selection in these species uncertain. Male body size might influence female fecundity even in die absence of assortadve mating for body size, as is die case in the present study. It seems, therefore, that studies of trade-offs between die components of LRS are still required as a means of demonstrating stabilizing selection, a view shared by Andersson (1994: 440) in his review of sexual selection: "no empirical study has yet shown quantitatively what compromise trait size R_ M. Neemi U now at 27 Bridge End, Foxen Lane, MiUbmk, Sowerby Bridge, HX6 3EQ, UK. Address correspondence to J. Lazarus. Received 18 November 1996; first revision 7 August 1997; second reviaon 27 October 1997; accepted 1 November 1997. O 1998 International Society for Behavioral Ecology is favored by the enhancing and opposing selection pressures that are likely to work in concert." We report here that in die swarming midge Chironomus plumosus small males have greater mating success and large males have greater stamina, fecundity, and longevity. LRS is greatest in males of intermediate size, and optimal size is close to the commonest size classes in die field, providing evidence for stabilizing selection. METHODS Male chironomids do not grow as adults and, because they are reproductive from eclosion, die effect of body size on fitness is not confounded by growdi or maturity. At dusk males form mating swarms to which females are attracted. A female flying into die swarm is grasped by a male, die pair leaves die swarm in copula, die female receives a spermatophore and she oviposits. Male chironomids feed during the day on widely dispersed "honeydew" (aphid secretion) but, since they probably do not compete over food, feeding success is unlikely to be influenced by body size (McLachlan, 1986b). We present new data here on fecundity, longevity, swarm size distributions, nonassortative mating, female behavior, spermatophore volume, and anatomical measurements of males and females relevant to sperm competition. Previously published data used here for the calculation of LRS and relevant methods are described by Neems et al. (1990, 1992). Body size was measured as wing length in millimeters (anal lobe to wing tip), a good indicator of body size in midges (McLachlan, 1986a). To measure fecundity, we captured mated pairs in the field and allowed die females to oviposit in the laboratory (once only, as in die wild). Pairs were captured, without disturbance, by placing a box over diem after diey landed on a sheet placed under die swarm. The pair was left undisturbed and dissociated naturally after about a minute. We placed a lid over die box and took the pair to die laboratory after diey •Department of Agricultural and Environmental Science, bDepartment of Psychology, and •"Department of Marine Sciences and Coastal Management, University of Newcastle upon Tyne, Newcastle upon Tyne, NE1 7RU, UK Behavioral Ecology Vol. 9 No. 3 280 RESULTS Components of lifetime reproductive success Lifetime reproductive success is determined by four components: daily mating probability, fecundity (number of offspring produced per mating), longevity, and stamina (which determines the time that males can remain in the mating swarm and therefore influences mating probability). Of die males that metamorphose into adults, all take part in the swarm except for the very smallest (i.e., 3.10-3.39 mm), which therefore do not mate (Neems, 1990; Neems et al, 1990). We assume that, apart from these smallest males, attendance in swarms is limited only by the male's ability to remain airborne. Daily mating probability in the swarm (mating success) Mating success as a function of body size (bs) and swarm size (N), M(bs,N), was calculated as die number of males of a given body size emerging from die swarm in mating pairs, MP(bsJV), divided by the total number in die swarm of die same body size, S(bsjf): (la) S(bs, (...truncated)