Individual sex ratios and offspring emergence patterns in a parasitoid wasp, Melittobia australica (Eulophidae), with superparasitism and lethal combat among sons

Since the mating of the parasitoid wasp Melittobia australica occurs on their eclosed hosts, the sex ratio is predicted to follow the local mate competition (LMC) theory. However, while LMC models predict that the sex ratio will increase from female-biased toward a 1:1 ratio with an increase in the number of foundresses, the observed female-biased sex ratios (1–5% males) show little increase in response to an increased foundress number. Lethal combat among adult males may serve as an explanation for this observed phenomenon. Using a microsatellite DNA marker, we first examined the individual sex ratio of two foundresses who had sequentially parasitized the same host. Both foundresses produced an extremely female-biased clutch and the sex ratios of the second foundress were only slightly less biased than that of the first. A small number of sons from both foundresses emerged at a constantly low rate over a prolonged period, resulting in a temporal mixture of emerging males derived from both the foundresses. Second, we conducted a one-on-one arena experiment to examine the combat level in relation to the relatedness of the opponents. Almost all the later-emerging males were killed by previously eclosed males irrespective of whether they were sibs or non-sibs. These results suggest that each foundress should not produce males in a single burst, but continue to produce male eggs at a constantly low rate in order to avoid the high mortality of her own sons by lethal male-male combat. This combat may be one of factors in explaining the extremely female-biased sex ratio even with an increasing foundress number.Communicated by R.F.A. Moritz     

Host choice and offspring sex allocation in a solitary parasitic wasp

Summary Females of the parasitic wasp Antrocephalus pandens can detect differences in the quality of their hosts (pupae of Corcyra cephalonica, a stored-product moth) and allocate offspring of either sex accordingly. Larger and younger hosts are accepted more often in both dead and live hosts; more female offspring emerge from the perceived better hosts, while more males emerge from the smaller, older ones. These patterns are consistent with a sex allocation strategy by the mother, since females from a given size host tend to be larger than males and larger females produce more eggs. However, when wasps lay their eggs in groups of hosts of different size and age rather than encountering them one at a time, no difference in number or sex ratio of offspring is detected between groups. This result and evidence from the change in offspring sex ratio with female age and with numbers of females foraging on a group of hosts are interpreted and discussed in the context of sex allocation (Charnov 1979) and local mate competition (LMC, Hamilton 1967) theories.     

Sex ratio responses to other parasitoid wasps: multiple adaptive explanations

In an effort to distinguish among adaptive models and to improve our understanding of behavioral mechanisms of sex ratio manipulation, this study examines sex ratio responses to other wasps in the solitary parasitoid wasp Spalangia cameroni. Relative to when alone, females produced a greater proportion of sons in the presence of conspecifics, regardless of whether the conspecifics were female or male. In addition, females produced a greater proportion of sons after a day with a conspecific male, and after a day with a conspecific female, but only if the females had been ovipositing. Relative to when alone, females did not produce a greater proportion of sons in the presence of females of the confamilial Muscidifurax raptor or in response to hosts that had already been parasitized by a conspecific. A combination of evolutionary models may explain S. cameroni’s sex ratios. An increased proportion of sons in response to conspecific females is common among parasitoid wasps and is usually explained by local mate competition (LMC) theory. However, such a response is also consistent with the perturbation model, although not with the constrained females model. The response to conspecific males is not consistent with LMC theory or the perturbation model but is consistent with the constrained females model.     

Local mate competition in the solitary parasitoid wasp <Emphasis Type="Italic">Ooencyrtus kuvanae</Emphasis>

Local mate competition (LMC) occurs when brothers compete with each other for mating opportunities, resulting in selection for a female-biased sex ratio within local groups. If multiple females oviposit in the same patch, their sons compete for mating opportunities with non-brothers. Females, in the presence of other females, should thus produce relatively more sons. Sex ratio theory also predicts a more female-biased sex ratio when ovipositing females are genetically related, and sex-ratio responses to foundress size if it differentially affects fitness gains from sons versus daughters. The mating system of the parasitoid wasp Ooencyrtus kuvanae meets assumptions of LMC. Females insert a single egg into each accessible egg of gypsy moth, Lymantria dispar, host egg masses. Wasps complete development inside host eggs and emerge en masse, as sexually mature adults, resulting in intense competition among brothers. We tested the hypothesis that O. kuvanae exhibits LMC by manipulating the number of wasp foundresses on egg masses with identical numbers of eggs. As predicted by LMC theory, with increasing numbers of wasp foundresses on an egg mass, the proportions of emerging sons increased. In contrast, the presence of a sibling compared to a non-sibling female during oviposition, or the size of a female, did not affect the number or sex ratio of offspring produced. The O. kuvanae system differs from others in that larvae do not compete for local resources and thus do not distort the sex ratio in favor of sons. With no resource competition among O. kuvanae larvae, the sex ratio of emergent son and daughter wasps is due entirely to the sex allocation by ovipositing wasp foundresses on host egg masses.     

Asymmetric larval competition in the parasitoid wasp <Emphasis Type="Italic">Nasonia vitripennis</Emphasis>: a role in sex allocation?

Sex allocation theory offers excellent opportunities for testing how animals adjust their behaviour in response to environmental conditions. A major focus has been on instances of local mate competition (LMC), where female-biased broods are produced to maximise mating opportunities for sons. However, the predictions of LMC theory can be altered if there is both local competition for resources during development and an asymmetry between the competitive abilities of the sexes, as has been seen in animals ranging from wasps to birds. In this paper, we test the extent to which asymmetric larval competition alters the predictions of LMC theory in the parasitoid wasp Nasonia vitripennis. We found that the body size of both sexes was negatively correlated with the number of offspring developing within the host. Further, we found that when faced with high levels of competition, the body size of females, but not males, was influenced by the sex ratio of the competing offspring; females were smaller when a higher proportion of the brood was female. This asymmetric competition should favour less biased sex ratios than are predicted by standard LMC theory. We then develop a theoretical model that can be parameterised with our data, allowing us to determine the quantitative consequences of the observed level of asymmetric larval competition for sex allocation. We found that although asymmetric competition selects for less biased sex ratios, this effect is negligible compared to LMC. Furthermore, a similar conclusion is reached when we re-analyse existing data from another parasitoid species where asymmetric larval competition has been observed; Bracon hebetor. Consequently, we suspect that asymmetric larval competition will have its greatest influence on sex ratio evolution in species that have smaller clutches and where local mate competition is not an issue, such as birds and mammals.     

Sex allocation and local mate competition in Old World non-pollinating fig wasps

The populations of many species are structured such that mating is not random and occurs between members of local patches. When patches are founded by a single female and all matings occur between siblings, brothers may compete with each other for matings with their sisters. This local mate competition (LMC) selects for a female-biased sex ratio, especially in species where females have control over offspring sex, as in the parasitic Hymenoptera. Two factors are predicted to decrease the degree of female bias: (1) an increase in the number of foundress females in the patch and (2) an increase in the fraction of individuals mating after dispersal from the natal patch. Pollinating fig wasps are well known as classic examples of species where all matings occur in the local patch. We studied non-pollinating fig wasps, which are more diverse than the pollinating fig wasps and also provide natural experimental groups of species with different male morphologies that are linked to different mating structures. In this group of wasps, species with wingless males mate in the local patch (i.e. the fig fruit) while winged male species mate after dispersal. Species with both kinds of male have a mixture of local and non-local mating. Data from 44 species show that sex ratios (defined as the proportion of males) are in accordance with theoretical predictions: wingless male species<wing-dimorphic male species<winged male species. These results are also supported by a formal comparative analysis that controls for phylogeny. The foundress number is difficult to estimate directly for non-pollinating fig wasps but a robust indirect method leads to the prediction that foundress number, and hence sex ratio, should increase with the proportion of patches occupied in a crop. This result is supported strongly across 19 species with wingless males, but not across 8 species with winged males. The mean sex ratios for species with winged males are not significantly different from 0.5, and the absence of the correlation observed across species with wingless males may reflect weak selection to adjust the sex ratio in species whose population mating structure tends not to be subdivided. The same relationship is also predicted to occur within species if individual females adjust their sex ratios facultatively. This final prediction was not supported by data from a wingless male species, a male wing-dimorphic species or a winged male species. Received: 27 July 1998 / Received in revised form: 11 January 1999 / Accepted: 16 January 1999     

Precise sex ratios manifested by several encyrtid parasitoids (Hymenoptera: Encyrtidae) of brown soft scale, <Emphasis Type="Italic">Coccus hesperidum</Emphasis> L. (Hemiptera: Coccidae)

We examined whether several facultatively gregarious encyrtid (Hymenoptera: Encyrtidae) endoparasitoids of brown soft scale, Coccus hesperidum L., manifest precise sex allocation under field conditions. Metaphycus luteolus (Timberlake), Metaphycus angustifrons (Compere), Metaphycus stanleyi (Compere), and Microterys nietneri (Motshulsky) evince brood sex ratios that are female-biased and extremely precise (low variance in the number of sons per host). Typically, this sex allocation pattern is attributed to extreme local mate competition (LMC) in which only one foundress exploits a patch of hosts and mating occurs mostly between her offspring. However, such a pattern of sex allocation was not detected for Metaphycus helvolus (Compere). Also, a large proportion of the broods in all five species contained only daughters; thus, an excess of male-only broods was expected if unmated females (i.e., females that can produce only sons) contribute offspring before mating. All-male broods were rare in our samples. This finding coupled with the life history characteristics of these wasps, such as the exploitation of aggregated hosts and the long life span and mobility of males, suggest that nonlocal mating is frequent. Our empirical work suggests that it is advantageous to allocate precise sex ratios in cases in which mating opportunities for males are not restricted to their natal host and/or when multiple foundresses exploit large patches of hosts. Limited theoretical work also supports this prediction but more detailed studies of this taxon’s mating structure and other life history characteristics are necessary to understand their sex allocation decisions.     

Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs

Telenomus fariai is a gregarious endoparasitoid of the eggs of several species of Triatominae (Hemiptera) with a high degree of sibmating: males fertilize their sisters inside the host egg before emergence or emerge first and copulate with their sisters as these emerge. Our results show that, when laying alone, T. fariai behaves adaptively, minimizing offspring mortality and conforming to the prediction of local mate competition (LMC) theory by laying a single male, which is sufficient to fertilize all the sisters. When more than one wasp was placed with one host, sex ratios still conformed to LMC predictions but, despite the decreasing number of eggs laid per wasp, clutch size could not be completely adjusted to avoid mortality. This is not surprising, as superparasitism is rare in the field. Offspring production was independent of the contacts between conspecifics but was affected by the number of mothers laying on a single host egg. The sex of the progeny was precisely determined: a female produced one male per clutch when laying on both unparasitized or previously parasitized hosts. On the other hand, a mother produced less daughters when superparasitizing. Under crowded conditions, the number of eggs laid per female wasp and per host decreased as the number of mothers increased. Developmental mortality also increased with the number of T. fariai eggs per host, determining a maximum of approximately 14 emerged adults. Host resources per individual affected male and female adult size with similar intensity, and male adult mortality was slightly higher than that for females. These results, and previous findings, suggest that T. fariai attains Hamiltonian sex ratios by laying one male and a variable number of females, and that the detection of chemical marks left by conspecifics provides information on the number of foundresses sharing a patch. Received: 4 February 2000 / Received in revised form: 19 April 2000 / Accepted: 20 May 2000     

Sex ratio and host size in a parasitoid wasp

Summary Parasitoid wasps often lay male eggs in small hosts and female eggs in larger hosts. The selective advantage of this strategy can be explained by assuming wasp fitness increases with host size and that this fitness increase is greater in females than in males. I conducted experiments to test a model based on this explanation and found the results generally supported the model with one exception; unlike what the model assumed, these wasps were unable to adjust their offspring sex ratios in each generation to different host size distributions. This finding suggests an alternate view as to how selection might operate in the evolution of parasitoid sex ratios.     

Sex ratio response to conspecifics in a parasitoid wasp: test of a prediction of local mate competition theory and alternative hypotheses

Maternal manipulation of offspring sex ratio in response to conspecifics is considered in relation to sex ratio theory using the parasitoid wasp Spalangia endius. Females produced a greater proportion of sons in response to mated but not virgin females. This is the first demonstration of a differential sex ratio response to virgin versus mated females and provides support for local mate competition theory. More recent sex ratio models that predict sex ratio responses to conspecifics, specifically constrained, perturbation, and crowding models, were not supported. An increased proportion of sons in response to another mated female occurred on the second day of oviposition but not on the first, and the day effect resulted from experience not age. When females oviposited alone after 2 days' exposure to another female, they still produced a greater proportion of sons than if they had always been alone, but only if the other female was mated, not if she was virgin. Females do not seem to assess the presence of virgin versus mated females indirectly by using a low density of males or a long latency to mate as an indicator for virgin females: neither affected offspring sex ratio. That mated females adjusted their sex ratios in response to other mated females, but not virgin females or males, may be due proximally to mated females not often encountering the latter. Virgin females and males are not located as deep in the oviposition substrate as mated females.     

Worker policing and nest mate recognition in the ant <Emphasis Type="Italic">Formica fusca</Emphasis>

A conflict over male production arises in social insects where workers are able to lay unfertilized male eggs. This happens because each female (queen or worker) is most closely related to her own sons and is thus predicted to reproduce. The conflict is modulated by worker policing where workers prevent each other from reproducing by aggression or egg cannibalism. In this study, we show that in the ant Formica fusca, worker policing occurs by egg cannibalism rather than by overt aggression among workers. Furthermore, we show that, contrary to bees, wasps and other ant species, egg discrimination in F. fusca is not based only on a universal queen signature chemical and that nest mate recognition of eggs occurs.     

Interspecific interference competition and mate choice in the soldier beetle,Chauliognathus pennsylvanicus

Summary Interference competition directed at soldier beetles, Chauliognathus pennsylvanicus, by four aggressive wasp species changed the mate choice of females. In the absence of wasps, females mated more frequently with males of greater weight and greater antennal scape diameter. Only in the presence of wasps did females frequently mate when they did not contain mature ova. When wasps were abundant, the proportion of beetles mating was higher. Wasps reacted aggressively toward mating beetles less frequently than toward single beetles. Therefore, females may have fed more efficiently in the presence of wasps when coupled.     

Sperm competition in the mite Caloglyphus berlesei

Summary The sperm utilisation pattern of C. berlesei was investigated using the sterile male method. The last male to mate with a female fertilised most of her eggs. In experiments where females mated with two virgin males, second males fertilised on average 86% of eggs when second matings took place immediately after the first. Last male sperm priority was also confirmed in experiments where females mated sequentially with three males. The proportion of eggs fertilised by the second male decreased to 71% and 56% when the interval between matings was 2 and 6 h, respectively. Males that had opportunities to mate prior to experiments copulated for a shorter time than virgin males, and second males fertilised on average 74% eggs.     

Condition-dependent sex allocation by clones of a galling aphid

Local mate competition (LMC) has been postulated to be the primary factor of female-biased sex allocation. In animals such as aphids that exhibit seasonal alternations of clonal and sexual reproduction, there is a high possibility of intra-clonal mating and LMC. This possibility is more plausible for more fecund clones, but outbreeding is predicted for less fecund clones. We hypothesize that clones that are more fecund will gain higher fitness returns by reducing investment in males because of more intense LMC among clonal males. We tested this hypothesis by elucidating the clonal sex allocation patterns of the galling aphid Kaltenbachiella japonica, in which inbreeding and LMC appear to be common. Winged mothers that emerge from a gall, belonging to the same clone, produced males and sexual females asexually on a branch, without dispersing to other trees. The heavier the gall, the more winged mothers were produced from the gall. Individual mothers produced a constant number of males and a variable number of females. The clonal sex allocation to males was 39.8?%, on average, and decreased with increasing gall weight. This result showed that clones that were more fecund exhibited more female-biased sex allocation and thus supported our hypothesis. Furthermore, our results corroborated Stubblefield and Seger’s hypothesis for sex allocation in patch structure rather than Yamaguchi’s constant male hypothesis. We conclude that K. japonica clones are able to adjust their sex allocation patterns adaptively depending on the quality of resources in the galls.     

Test of the adaptiveness of sex ratio manipulation in a parasitoid wasp

In behavioral ecology it is generally assumed that behavior is adaptive. This assumption is tested here for sex ratio manipulation in response to host size in the parasitoid wasp Spalangia cameroni. Females produce a greater proportion of daughters on larger hosts. If this behavior is adaptive, it is not through a positive effect of host size on the fitness of daughters, as theory suggests and as found for other species. Females that developed on larger hosts were not more successful at drilling into hosts, were not more successful at interspecific competition for hosts, and did not have greater dispersal ability as measured by wing loading (weight/area of wing and thorax). The possibility that S. cameroni's sex ratio manipulation may be adaptive through a negative effect of host size on the fitness of sons cannot be ruled out. Relative to males from larger hosts, males from smaller hosts had lower wing loading and thus potentially greater dispersal ability. The actual effect of wing loading on fitness remains to be tested.     

Local mate competition,sex ratio and clutch size in bethylid wasps

Summary Parasitoid wasps of the family Bethylidae lay groups of eggs on the larvae of beetles and moths. The larvae develop together and pupate in the vicinity of the host. On hatching, the majority of copulations are between siblings leading to a high degree of local mate competition. Sex ratio theory predicts that as the number of individuals developing on a host increases, the population sex ratio will become progressively more female biassed. A comparative study of sex ratios across the family supports this prediction.     

Precise sex allocation, local mate competition, and sex ratio shifts in the parasitoid wasp Trichogramma pretiosum

We determined the sex, order, and clutch size of eggs laid by the parasitoid wasp, Trichogramma pretiosum Riley, in the eggs of one of its natural hosts, Trichoplusia ni (Hübner). The parasitoid allocated sex non-randomly to hosts in the laboratory with a variance significantly less than that of a binomial (random) distribution, our null model. More clutches of two or more eggs contained a single male egg as the second or third egg laid than would be expected by chance and none contained two or more male eggs. T. pretiosum also increased the sex ratio (% male) of its offspring with increasing foundress numbers by increasing the frequency of male offspring as the second egg in a two-egg clutch allocated to unparasitized hosts and as the single egg allocated to previously parasitized hosts. These results indicate that T. pretiosum allocates the sex of its offspring precisely. Precise sex allocation is favored under local mate competition because it reduces variation in the number of sons per patch thus maximizing the number of inseminated daughters emigrating from the patch. Similar combinations of female and male offspring emerged from T. ni eggs parasitized by T. pretiosum in the field, again with a sex ratio variance less than that expected for a binomial distribution. These results strongly suggest that this parasitoid species manifests local mate competition.     

Sex ratio, sexual dimorphism and mating structure in bethylid wasps

Sexual dimorphism has been linked to parasitoid mating structure by several authors. In turn mating structure has an important influence on predicted sex ratio optima. Here we test the relationship between sexual dimorphism and sex ratio using data from 19 species of bethylid wasps. Using phylogenetically based comparative methods we confirm the findings of a previous cross-species analysis that sex ratio (proportion of males) is strongly and negatively correlated with clutch size. Using cross-species comparisons we show an additional positive correlation of sex ratio and relative male size, as predicted. The relationship however is not significant when using phylogenetically based methods. The cross-species result is largely due to differences between two bethylid sub-families: the Epyrinae have relatively large males and relatively high sex ratios, whereas the Bethylinae have relatively small males and lower sex ratios. Our study illustrates the benefits and drawbacks of using cross-species versus phylogenetically based comparisons. Received: 13 May 1997 / Accepted after revision: 12 January 1998     

Male choice and competition in Tetraopes tetraophthalmus: effects of local sex ratio variation

Summary Male milkweed beetles (Tetraopes tetraophthalmus) are shown to exhibit choice between potential mates. Males, however, also exhibit direct competition for access to potential mates. These differences in male behavior are dependent on the local sex ratio, with males becoming increasingly choosy when the sex ratio is female-biased, and more competitive when the sex ratio is malebiased. Females show neither choice nor competition. In both the laboratory and in the field, body size is important in determining patterns of competition and choice. Larger males win most aggressive encounters, and males generally prefer large females as mates. The combination in a single sex, of competition for mates and mate choice is not predicted by classical sexual selection theory. Male choice and competition may have evolved in T. tetraophthalmus due to the combination of (1) the mating system (2) the pattern of variation in female fecundity, and (3) the spatially and temporally variable operational sex ratios. This explanation is not dependent on high heritability of body size.     

Parental care and mate attraction in the Florida flagfish, <Emphasis Type="Italic">Jordanella floridae</Emphasis>

Theory suggests that there is a trade-off between mate attraction and investment in parental care. Yet, under some circumstances, such as in species with uniparental male care, it is conceivable that males who provide more care also attract more females, and hence avoid this cost. We tested these two alternative hypotheses using the Florida flagfish, Jordanella floridae, which is a highly sexually dimorphic species with male parental care. We predicted that if components of male care behavior primarily serve offspring survival, they should display these behaviors more in the presence of eggs than without eggs. We also predicted that males should show a trade-off between display, and other activities directed to other fish, and care behaviors. Alternatively, if care has a positive effect on mating success, we expected males to show care even in the absence of eggs, and that they should display more care in the presence of females. We found that care behavior mostly depended on the presence of eggs, males increased care when they guarded eggs, and there was a negative relationship between rates of interaction and care behavior. Most care was exhibited in the absence of other fish while the presence of males and females both had a negative effect on care behavior. There was no difference in care behavior with males or females present. Only nest-visitation rates were highest in the presence of females, suggesting that this behavior is used as part of the courtship. These results support the idea that male care in this species is primarily influenced by natural selection. Males did, however, display fanning and other egg-directed behaviors even in the absence of eggs. The level of these behaviors was constant and independent of display behavior. Hence, it seems that care may be used in mate attraction before the male has received his first clutches.