Behavioral Ecology Vol. 14 No. 1: 34-39
© 2003 International Society for Behavioral Ecology
Extremely female-biased sex ratio and lethal male–male combat in a parasitoid wasp, Melittobia australica (Eulophidae)
aDepartment of Systems Sciences (Biology), University of Tokyo, Meguro, Tokyo 153-8902, Japan bDepartment of Biology, Tokyo Metropolitan University, Minamiosawa 1–1, Hachioji, Tokyo 192-0397, Japan
Address correspondence to J. Abe. E-mail: abej{at}dolphin.c.u-tokyo.ac.jp.
Received 18 September 2001; revised 19 March 2002; accepted 23 April 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Melittobia australica (Hymenoptera: Eulophidae) is a gregarious ectoparasitoid of the prepupae and pupae of solitary wasps and bees. The males never disperse from their natal patch, and mating takes place only on the host from which they emerged. We measured the offspring sex ratio of M. australica with differing foundress numbers and examined combat between emerged males. The offspring sex ratios were extremely female biased and almost independent of foundress number in all cases. The population of M. australica used in the experiment was infected with the cytoplasmically inherited symbiotic bacterium Wolbachia. However, although Wolbachia is a potential sex-ratio distorter, noninfected individuals showed the same sex ratio patterns as the Wolbachia-infected individuals. An arena experiment showed that younger males were almost always killed by older males that had eclosed earlier. These results suggested that lethal male–male combat is an additional factor distorting the sex ratio toward a more female-biased sex ratio. This provides a new perspective on current local mate competition models.
Key words: local mate competition, male–male combat, Melittobia australica, parasitoid wasps, sex ratios, Wolbachia.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Local mate competition (LMC) is said to occur when brothers compete for matings with their sisters. This competition selects for a female-biased sex ratio because a female can maximize her fitness by ovipositing the minimum number of males necessary to ensure that all female offspring are mated (Hamilton, 1967
). Moreover, inbreeding results in inheritance asymmetry between sons and daughters in haplodiploid species (where males are haploid and produced from unfertilized eggs, while females are diploid and produced from fertilized eggs), and this asymmetry causes a slightly more female-biased sex ratio (Frank, 1985; Hamilton, 1979; Herre, 1985). The relative importance of LMC and of inbreeding depends on the number of foundresses that oviposit in a local patch. Theoretical studies have predicted that the optimal sex ratio (defined as proportion of males) will increase toward 50% with increasing numbers of foundresses (Frank, 1985; Hamilton, 1979; Herre, 1985). The predictions of LMC theory have explained well cases in which the number of foundresses varies in a patch, as found in many fig wasps (Frank, 1985; Hamilton, 1979; Herre, 1985, 1987) and in many parasitoid wasps (Werren, 1983; reviewed by Godfray, 1994; Godfray and Cook, 1997; King, 1987).
Melittobia australica Girault (Hymenoptera: Eulophidae) is a gregarious ectoparasitic parasitoid wasp, and its primary hosts are the prepupae and pupae of solitary wasps and bees nesting above the ground (Browne, 1922; Maeta and Yamane, 1974). Extreme sexual dimorphism occurs in this genus (Browne, 1922; Dahms, 1984); females have fully developed wings and eyes, whereas males are brachypterous (i.e., with nonfunctional, short wings), lack compound eyes, and show less dark pigmentation than found in the females. Matings take place within the host cocoon or puparium from which the offspring emerge (Browne, 1922; Buckell, 1928; Iwata and Tachikawa, 1966). When we checked the spermatheca of dispersing females from their host cocoons, all females examined had sperm (Abe, unpublished data; see also Browne, 1922), which suggested that each female disperses after mating in nature. Only mated females disperse to seek a new host, whereas males never leave the host cocoon or puparium, spending their entire life inside (Browne, 1922). Thus, LMC theory should be applicable to Melittobia. Although Melittobia was included in the list of species potentially exhibiting LMC by Hamilton (1967), there has been little attention paid to their sex-ratio patterns (but see Freeman and Ittyeipe, 1982).
A host individual may be often attacked by more than one Melittobia female in the field (Freeman and Ittyeipe, 1976; van den Assem et al., 1980). The adult males are extremely pugnacious and fight fiercely with one another. They have scythe-shaped mandibles which prove to be an effective weapon for chopping off limbs and the head of opponents (Godfray and Cook, 1997; van den Assem et al., 1980). This lethal combat may be an additional factor of the female-biased sex ratio in Melittobia.
In addition, it has been reported that Melittobia is infected with the cytoplasmically symbiotic bacterium, Wolbachia (Werren et al., 1995). Wolbachia, which is maternally inherited and widely infects arthropods and nematodes, sometimes distorts the sex ratio of its hosts toward females in various ways, such as parthenogenesis (Stouthamer, 1997; Stouthamer etal., 1990), feminization of genetic males (Kageyama et al., 1998; Rigaud, 1997; Rigaud et al., 1997), and male killing (Hurst etal., 1999). This increases its own transmission through a host population.
Thus, aims of this study were to test the hypotheses that sex ratios of M. australica vary with respect to (1) the number of foundresses that parasitize a host, (2) Wolbachia infection, and (3) lethal combat among adult males. We demonstrate that lethal male–male combat is a novel factor distorting the offspring sex ratio toward females.
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METHODS |
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An experimental population of M. australica was established from wasps that emerged from Megachile sculpturalis Smithprepupae in Hachioji City, Tokyo, Japan, in 1999. The parasitoid stock cultures were reared in plastic cages (90 mm diam, 30 mm high), each of which was ventilated by an 8-mm hole covered in 120-mesh steel gauge (Freeman and Ittyeipe, 1993
). They were kept under conditions of 25°C and 16 h light: 8 h dark photoperiod. M. sculpruralis prepupae were maintained in cooled, diapause condition and used for hosts in stock cultures and experiments.
Generating Wolbachia-free and Wolbachia-infected strains
We randomly selected 100 M. australica females from one stock culture at a time and divided them into two subpopulations to establish Wolbachia-free (W-) and Wolbachia-infected (W+) strains. To generate the W- strain, each of 50 females was allowed to parasitize a host that had been injected with about 40 µl of tetracycline solution (140 µg/ml tetracycline, 800 mg NaCl, 20 mg KCl, 115 mg NaHPO4, 20 mg KH2PO4 in 100 ml distilled water). To eliminate the effects of tetracycline on parasitoid development, nontreated hosts were parasitized by female adults that had emerged from the tetracycline-injected host, and newly emerging parasitoids in the next generation were used for the sex ratio experiment. Another 50 females were each allowed to oviposit on a normal, untreated host. With the exception of the tetracycline treatment,W+ strains were reared in exactly the same fashion as the W- wasps.
We determined the presence or absence of Wolbachia in a parasitoid by diagnostic polymerase chain reaction amplification of Wolbachia surface protein gene fragment (wsp) (Zhou et al., 1998). A 0.6-kb fragment of this gene was amplified using a set of primers wspF [5'-GGGTCCAATAAGTGATGAAGAAAC-3'] and wspR [5'-TTAAAACGCTACTCCAGCTTCTGC-3'] with cycles of 1 min at 94°C, 1 min at 50°C, and 1 min at 70°C (Kondo et al., 2002). Amplification of a portion of mitochondrial 16S rRNA gene was used as a positive control to verify template quality. A fragment of just <0.4 kb was amplified using the primers 16SF [5'-TTACGCTGTTATCCCTAA-3'] and 16SR [5'-CGCCTGTTTATCAAAAACAT-3'] with cycles of 30 s at 93°C, 1 min at 47°C, and 1 min 15 s at 72°C (Kambhampati and Charlton, 1999). From these polymerase chain reaction amplifications, we confirmed that Wolbachia existed in the strain untreated with tetracycline but was not present in the treated strain. As positive control, both strains exhibited the amplified Melittobia mitochondrial 16S rRNA gene.
Sex ratio experiment
To compare sex allocation responses of the two (W+ and W-) strains to the number of foundresses in one host, either 1, 2, 4, 8, or 16 newly emerged female wasps of each strain were introduced into the plastic cage (90 mm diam, 30 mm high) with one host and were allowed to oviposit freely for 12 days. We made five replicates for each foundress abundance for each of the two strains. These foundresses had emerged from different hosts on each of which a different female had oviposited (i.e., the foundresses were nonsiblings). After 12 days, all foundresses were removed, and their DNA was isolated to confirm the presence of Wolbachia.
Newly emerged offspring wasps from each plastic cage were sexed and removed on a daily basis until every wasp emerged. We were able to obtain the offspring number before lethal combat among adult males, as previously emerged males had been removed as soon as they emerged. The offspring sex ratio of each plastic cage was obtained by summing the total numbers of each sex.
Because of the haplodiploid sex determination, we need to confirm whether the foundresses had been fertilized. Females that belonged to the same cohort as the foundresses were removed from a subculture at the same time as the foundress collection and were dissected in phosphate-buffered salinesolution (800 mg NaCl, 20 mg KCl, 115 mg NaHPO4, 20 mg KH2PO4 in 100 ml distilled water) under a binocular microscope. We confirmed the presence or absence of spermin their spermatheca under a light microscope to determine if they had been mated (W+ strain, n = 173; W- strain, n = 194).
Male–male combat
We conducted an arena experiment to determine whether an already emerged adult male or a subsequently eclosed male will defeat the opponent in the lethal combat. We collected 206 M. australica males of the late pupal stage from the subcultures (W+ strain). We marked 105 newly emerged males on the dorsal side of the abdomen with permanent marker and were divided into two groups. The first group of53males was individually introduced into an arena (each 4.5 mm diam, 2 mm high; made of paper and glass) together with a pupal male. The two males had been collected from different hosts on each of which a different female had oviposited (i.e., the males were nonsiblings). The pupal males eclosed 1–3 days after the experiment commenced. We recorded the date when the pupal male emerged and the date when either male died, until both the males died. As the control, we introduced individually either another 52 marked adult males (the second group) or 48 pupal males into individual arenas, and their adult longevity was measured in a similar manner.
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RESULTS |
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Sex ratio experiment
All females examined had sperm in their spermatheca. The foundresses that had been introduced into the plastic cage wandered about inside the cage for the first few days. They then remained on the host until they were removed on day 12, as long as their offspring larvae did not cover the host's surface. Daily spot sampling showed that every foundress in a plastic cage remained on the host and successfully parasitized the host. Offspring eclosed between 15 and 39 days after the introduction of the foundresses. Males eclosed significantly earlier than females in most cases (Figure 1; Kolmogrov-Smirnov test; all p values <.001, except for the one-foundress treatment of W+ strain,
2 = 6.35, df = 2, marginal difference p =.038 and for the one-foundress treatment of W- strain, 2 = 1.00, df = 2, no significant difference p =.605). Adult emergence finished earlier in the 8- and 16-foundresses treatments due to host resource depletion.
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The total brood size increased significantly with increasingthe number of foundresses in both W+ and W- strains (Figure 2A; Spearman rank correlation, rs =.946, n = 24, p <.001; rs= 0.886, n = 21, p <.01, respectively). When the data were grouped into classes based on foundress number, significant differences were found (ANOVA, F = 19.460, df = 4,19, p <.001; F = 11.435, df = 4,16, p <.001,respectively). The sex ratio increased slightly (but significantly) with increasing number of foundresses in both W+ and W- strains (Figure 2B; Spearman rank correlation, rs =.859, n = 24, p<.001; rs=.643, n=21, p <.01, respectively). When the sexratio data were also grouped into classes based on foundressnumber, significant and marginal differences were found in W+ and W- strains, respectively (Kruskal-Wallis test, H= 19.316, p <.001; H = 9.058, p =.060, respectively). No significant differences in the median sex ratio between W+ andW- strains for all the foundress abundances were found (Figure2B; Mann-Whitney U test, p >.076), except for the two-foundressestreatment (U = 1, p =.043). Sex ratio was consistently much more extremely female biased than the LMCmodel prediction in Figure 2B [(n – 1) (4n – 2)/n(4n – 1) where n is number of foundresses; Hamilton, 1979
]. Even if these observed sex ratios were compared with a prediction ofthe LMC model in a completely inbred species, (n-1)/3n(Frank, 1985; Herre, 1985; Werren, 1987), the predicted value was much higher than the 99% confidence limit (Figure2B).
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Male–male combat
No significant difference was found between the longevities of the two males types in the controls (Figure 3A; the median was 21 days for the initially eclosed male and 23 days for the subsequently eclosed male; Mann-Whitney U test, U = 917, p =.951). When a marked adult male and a pupal male were introduced together in an arena, almost all the previously eclosed adult males survived much longer than their younger opponent (Figure 3B). Only 5.7% (3/53) of the latter males survived longer. A pairwise comparison of the two males revealed that the previously eclosed males had significantly greater longevity than the later ones (Wilcoxon paired test, n=52, p <.001). The males often pounced on the opponents immediately after or during the act of the later male's eclosion. In many cases, the head, abdomen, antennae, or limbs of dead males were cut off by the victor. The median longevity of the initially eclosed male was 22 days, which was not significantly different from that of the control (U = 1310, p =.663). In contrast, the longevity of the later eclosed (i.e., pupal) males (the median was 0 days) decreased markedly when compared to that of the control (U = 2, p <.001). Moreover, the mortality during the pupal stage was much higher than in the control (Figure 3B). All of these results show that the pupal male was almost always killed by the already eclosed male immediately after, or even before, eclosion.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sex ratio pattern in Melittobia and LMC
The experimental manipulation of foundress number parasitizing the same host resulted in hardly any change in sex ratios in response to an increasing number of foundresses (Figure 2B; see also Wilhelm P, unpublished, cited in Werren, 1987
). Because the method of measuring offspring sex ratios involved the daily removal of newly emerged adults, the results do not include the effect of differential mortality through lethal combat among adult males. This result was contrary to current LMC theory (Hamilton, 1967, 1979). Although a number of studies have supported LMC predictions, at least qualitatively, in fig wasps (reviewed by Herre et al., 1997; slightly shifted sex ratio for some pollinating fig wasps: Herre, 1987; Herre et al., 1997; Kinoshita et al., 1998) and in parasitoid wasps (reviewed by Godfray, 1994; Godfray and Cook, 1997; King, 1987), we are not aware of any studies showing that sex ratio was almost wholly independent of foundress number (except for nonpollinating fig wasps having wingless males: Fellowes et al., 1999; but see also King, 1989).
Parasitoid wasps are not necessarily able to facultatively change the offspring sex ratio depending on the number of foundresses in a patch (Werren, 1987). If a host is rarely parasitized by more than one foundress, or if the wasp lacks an ability to assess the foundress number, a fixed optimal sex ratio would evolve in response to the expected average level of LMC and inbreeding in the population (Nunney and Luck, 1988; see also Fellowes et al., 1999; Werren, 1987). Herre (1987) showed the deviations from the optimal sex ratio predicted by LMC for the one- or two-foundress case in 13 fig wasp species. The deviations are least in the species that most frequently encounter that number of foundresses in nature, and females alter their offspring sex ratio more in response to different foundress number in the species that encounter more variable LMC situations (see also Herre et al., 1997; West et al., 2000). However, in Melittobia, notwithstanding that more than one female may often attack a host in nature (Freeman, 1977; Freeman and Ittyeipe, 1976; van den Assem et al., 1980), the natural sex ratio was extremely female-biased (almost 2–3% in Figure 2B; see also Maeta, 1978). Therefore, it is impossible to explain the sex allocation pattern of Melittobia with only LMC and inbreeding models.
Other potential factors influencing the sex ratio pattern
Wolbachia is a possible candidate as a female-biased sex-ratio distorter. Although Wolbachia infection was detected in this study in M. australica using diagnostic polymerase chain reaction amplification, the Wolbachia-free (W-) strain had essentially the same sex ratio (Figure 2) as the Wolbachia-infected (W+) one. This result showed that Wolbachia infection does not affect the sex ratio of M. australica.
Three other reasons the sex ratio may be more female biased than predicted by LMC theory have been suggested. First, if genetic similarity exists among foundresses ovipositing on the same host, a more female-biased sex ratio may be adaptive because related sons have an additional chance of mating with related females (Frank, 1985; Grafen, 1984). However, limited dispersal that leads to foundresses being related also increases local competition for resources among related females, and the two opposing factors are likely to cancel each other out (Frank, 1998; Queller, 1994; Taylor, 1992). Therefore, a female-biased sex ratio is not expected to evolve in this situation. Second, variable brood sizes by different foundresses make the sex ratio more female biased, so that the number of effective foundresses is reduced (Frank, 1985). However, only with enormous differences in brood size could this effect account for the sex ratio pattern of Melittobia. Third, differential mortality between male and female is likely to have a great effect on the observed sex ratio pattern (Godfray, 1994). An increase in the foundress number will lead to greater competition among larvae on a host. If male larvae suffer greater mortality before emergence, a female-biased sex ratio would be observed at emergence. Testing this idea would require measuring the primary sex ratio by using the karyotype difference found between the sexes in haplodiploids, for example. However, this effect is not likely to account for the observed sex ratio pattern because the mortalities of the multiple foundresses broods do not increase with the rise in foundress number, at least when foundress number is eight or fewer (Figure 2A).
Lethal male–male combat in Melittobia
This study focuses on the effect of lethal male–male combat as a novel possible factor distorting the sex ratio toward a female bias in Melittobia. The male–male combat experiment showed that later-emerging males were killed by already eclosed males in almost all cases (Figure 3). A foundress ovipositing on a previously attacked host may refrain from producing male offspring, as these later-emerging males will be killed by older males. Therefore, the sex ratio at oviposition may be predicted to be female biased even in superparasitism. Melittobia is ectoparasitoid, meaning that the eggs and developing larvae remain on the host surface. Therefore, a newly arrived potential foundress is likely to recognize whether the host is previously parasitized or not. Suzuki and Iwasa (1980) and Werren (1980) predicted, based on evolutionarily stable strategy (ESS) sex-ratio models for two foundresses sequentially parasitizing the same host, that the second foundress should produce relatively many more males than the first one. However, their model did not include lethal male–male combat. If this factor is included in the ESS model, the later foundress may avoid producing male offspring to maximize her fitness. We are analyzing the validity of this hypothesis with an ESS model (Abe et al., unpublished data). Previous LMC models (Hamilton, 1967, 1979) have implicitly assumed that all sons produced by foundresses have an equal opportunity to mate. However, in Melittobia, sons from the first foundress have a great advantage regarding mating opportunities due to the male–male combat. Genetic markers, such as microsatellite DNA, are needed to distinguish the offspring sex ratio of different females, especially the first and second foundresses, in further work.
Some nonpollinating fig wasps exhibit consistently more female-biased sex ratios than predicted by the LMC model (Herre et al., 1997), and lethal combat is seen among males (Frank, 1987; Hamilton, 1979; see also Murray, 1987, 1989). Therefore, the effect of lethal male–male combat as seen in Melittobia could be broadly applicable in LMC theory, and further development of the theory will be required. In addition, because the localized scale of competition (West et al., 2001) could help explain fierce competition between the highly related adult males of Melittobia, further research on this aspect is also required in the future.
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ACKNOWLEDGEMENTS |
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We thank T. Suzuki, T. Kusano, F. Hayashi, and members of our laboratory for helpful advice during this study. We also thank Y. Maeta for identifying species name of the parasitoid. We are grateful to M.D.E. Fellowes, A. F. G. Bourke, S. A. West, and an anonymous referee for valuable comments on the manuscript.
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