Sex ratios under asymmetrical local mate competition in the parasitoid wasp Nasonia vitripennis

Sex ratio theory has proved remarkably useful in testing theadaptive nature of animal behavior. A particularly productivearea in this respect is Hamilton's theory of local mate competition(LMC), which has been extended in numerous directions to includegreater biological realism, allowing more detailed tests inspecific organisms. We have presented one such extension, termedasymmetrical LMC, which occurs when egg laying by females ona patch is asynchronous, and emerging males do not disperse,resulting in the extent of LMC on a patch varying over time.Our aim here is to test whether the parasitoid wasp Nasoniavitripennis responds to variation in the degree of asymmetricalLMC. Specifically, we show that females adjust their offspringsex ratios in response to (1) variation in the amount of asynchronyin emergence between broods on a patch and (2) the number andproportion of previously parasitized hosts on the patch. Ourresults provide qualitative support for the predictions of theory,suggesting new levels of complexity in the sex ratio behaviorof this much-studied organism. However, our results do not alwaysprovide quantitative support for theory, suggesting furthercomplexities that must be clarified.     

Female-biased sex ratios under local mate competition: An experimental confirmation

Summary Experimental work of Nadel and Luck (1992) on a chalcidoid wasp provides a confirmation of sex ratio theory under local mate competition.     

Sex allocation of parasitic wasps: local mate competition,dispersal before mating and host quality variation

We constructed a sex allocation model for parasitic wasps to explain the wide variation in their sex ratio, considering the effects of local mate competition, partial dispersal of progeny before mating, and heterogeneity in host quality among patches. We conducted an experiment to compare with the predictions of our model. We considered the following situations. First, the hosts are distributed in discrete patches: a number of female wasps visit and oviposit in each patch. Second, all the progeny do not mate within the natal patch; some of them disperse to take part in population-wide random mating. We calculated ES sex ratios in cases where there are two kinds of patches: good ones and poor ones. We examined the dependency of ES sex ratios on several parameters, i.e., 1) the probability that a daughter mates in her natal patch, 2) the ratio of the female fitness of the good patch to that of the poor patch, 3) the proportion of poor patches, and 4) the number of foundresses in a patch. The result of our experiment showed the same tendency as the calculation in case where the LMC effect is high in each patch. We briefly discuss a possible selection pressure for dispersal of progeny, with special reference to the mating structure of parasitic wasps.     

Sex allocation in Epidinocarsis lopezi: local mate competition

Epidinocarsis lopezi is used as a biological control agent against the cassava mealybug, Phenacoccus manihoti, a serious pest of cassava in Africa. The efficiency of parasitoid mass-rearing is maximized when maximum numbers of healthy female wasps are obtained, since only female parasitoids attack the mealybugs.Highly variable sex ratios are often found in parasitic Hymenoptera. Local mate competition (LMC) is one of the evolutionary models which provide predictions about sex allocation. In this paper we show that E. lopezi does not respond to parasitoid density with a change in sex ratio. We also show that in the field, no local mating structure exists, and that mating is random. Therefore, a shift in sex ratio in response to parasitoid density as predicted by LMC theory would not be adaptive. E. lopezi also does not change its sex allocation when ovipositing in already parasitized hosts. Hence host-size distribution and differential mortality are the only factors that can influence sex ratio in mass-rearings.

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Résumé E. lopezi est utilisé dans la lutte biologique contre Phenacoccus manihoti, important ravageur du manioc en Afrique. Puisque seules les femelles du parasitoïde attaquent la cochenille, l'efficacité de l'élevage de masse de l'entomophage sera optimale quand le maximum de femelles saines sera obtenu.Les rapports des sexes des hyménoptères parasites varient très souvent. La compétition sexuelle locale (LMC) constitue l'un des modèles qui fournissent des prédictions de la distribution des sexes. Cette note montre que la proportion des sexes de E. lopezi n'est pas modifiée par la densité du parasitoïde. Par ailleurs, les accouplements s'effectuent au hasard dans la nature et il n'y a pas de structure locale d'accouplement. Par conséquent, le biais, prévu par la théorie du LMC, et introduit par la densité du parasitoïde dans la distribution des sexes, n'a pas de valeur adaptative. E. lopezi ne modifie pas non plus la distribution du sexe de ses descendants quant il pond dans de hôtes déjà parasités. Ainsi, la répartition en taille des hôtes et la mortalité différentielle sont les seuls facteurs qui influent sur la proportion des sexes dans les élevages de masse.

     

Sex allocation by a mite parasitic on insects: local mate competition,host quality and operational sex ratio

The aim of this study was to test the predictions of local mate competition (LMC), host quality (HQ) and operational sex ratio (OSR) models, using a non-arrhenotokous parasitic mite, Hemisarcoptes coccophagus (Astigmata: Hemisarcoptidae). The life-history pattern of this mite meets the assumptions of these sex allocation models. Mating group size (LMC model), HQ and OSR affected the sex allocation of H. coccophagus females. Only young mite females adjusted the sex ratio of their progenies according to the predictions of LMC and HQ models; the sex allocation of old females was contrary to these predictions. We explain these patterns by the dynamic nature of the mite's population structure. When parents are young, their population distribution is patchy and progeny matings are local; hence sex allocation is in accordance with LMC theory. When parents become older, their populations shift towards panmixis; factors which had operated previously no longer exist. Consequently, females adjust the sex ratio of late progenies so that it can compensate for the earlier sex allocation, in order to make their total sex ratio unbiased, as expected in panmictic populations. Our data, expressed as the cumulative sex ratio, support this hypothesis.     

Sex allocation of three solitary ectoparasitic wasp species on bean weevil larvae: Sex ratio change with host quality and local mate competition

Sex ratio manipulation by ovipositing females was surveyed in 3 solitary ectoparastic wasp species,Dinarmus basalis (Pteromalidae),Anisopteromalus calanrae (Pteromalidae), andHeterospilus prosopidis (Braconidae), that parasitize azuki bean weevil (Callosobruchus chinensis (L) (Coleoptera: Buruchidae)) larvae within azuki beans (Vigna angularis). Variables were local mate competition (LMC) and host quality (HQ). We used host age as a measure of host quality (from 9-to 16-day-old hosts), changed the number of ovipositing females to control the level of local mate competition (1 female and 10 females), and examined oviposition patterns of the wasps. The offspring sex ratios (proportion of females) of the 3 wasp species respond qualitatively same to HQ and LMC. The common qualitative tendency among the 3 species is an increase of sex ratios increase with host age. In the process of changing the sex ratio (9–13-day-old) 3 wasp species respond only to HQ. In the hosts that end development in size (14–16-day-old) wasps respond to LMC. The response of sex ratio change to LMC in the old host ageclasses are different among the 3 species. In the situation that there exists LMC (10 females) sex ratios are the same among the 3 wasps. However, the sex ratios in no LMC (single female) are heterogeneous among the 3 wasps.     

Evolution of extraordinary female-biased sex ratios: the optimal schedule of sex ratio in local mate competition

Female-biased sex ratio in local mate competition has been well studied both theoretically and experimentally. However, some experimental data show more female-biased sex ratios than the theoretical predictions by Hamilton [1967. Science 156, 477-488] and its descendants. Here we consider the following two effects: (1) lethal male-male combat and (2) time-dependent control (or schedule) of sex ratio. The former is denoted by a male mortality being an increasing function of the number of males. The optimal schedule is analytically obtained as an evolutionarily stable strategy (ESS) by using Pontrjagin's maximum principle. As a result, an ESS is a schedule where only males are produced first, then the proportion of females are gradually increased, and finally only females are produced. Total sex ratio (sex ratio averaged over the whole reproduction period) is more female-biased than the Hamilton's result if and only if the two effects work together. The bias is stronger when lethal male combat is severer or a reproduction period is longer. When male-male combat is very severe, the sex ratio can be extraordinary female-biased (less than 5%). The model assumptions and the results generally agree with experimental data on Melittobia wasps in which extraordinary female-biased sex ratio is observed. Our study might provide a new basis for the evolution of female-biased sex ratios in local mate competition.     

Evolution of sex ratios in social hymenoptera: kin selection,local mate competition,polyandry and kin recognition

A model is constructed to study the effects of local mate competition and multiple mating on the optimum allocation of resources between the male and female reproductive brood in social hymenopteran colonies from the ‘points of view’ of the queen (parental manipulation theory) as well as the workers (kin selection theory). Competition between pairs of alleles specifying different sex investment ratios is investigated in a game theoretic frame work. All other things being equal, local mate competition shifts the sex allocation ratio in favour of females both under queen and worker control. While multiple mating has no effect on the queen’s optimum investment ratio, it leads to a relatively male biased investment ratio under worker control. Under queen control a true Evolutionarily Stable Strategy(ess) does not exist but the ‘best’ strategy is merely immune from extinction. A trueess exists under worker control in colonies with singly mated queens but there is an asymmetry between the dominant and recessive alleles so that for some values of sex ratio a recessive allele goes to fixation but a dominant allele with the same properties fails to do so. Under multiple mating, again, a trueess does not exist but a frequency dependent region emerges. The best strategy here is one that is guaranteed fixation against any competing allele with a lower relative frequency. Our results emphasize the need to determine levels of local mate competition and multiple mating before drawing any conclusions regarding the outcome of queen-worker conflict in social hymenoptera. Multiple mating followed by sperm mixing, both of which are known to occur in social hymenoptera, lower average genetic relatedness between workers and their reproductive sisters. This not only shifts the optimum sex ratio from the workers’ ‘point of view’ in favour of males but also poses problems for the kin selection theory. We show that kin recognition resulting in the ability to invest in full but not in half sisters reverts the sex ratio back to that in the case of single mating and thus completely overcomes the hurdles for the operation of kin selection.     

Joint evolution of sex ratio and reproductive group size under local mate competition with inbreeding depression

Local mate competition (LMC) may involve some amount of inbreeding between siblings. Because sib-mating is generally accompanied by inbreeding depression, natural selection may favor a reduced rate of sib-mating, possibly affecting the evolution of sex ratio and reproductive group size. The present study theoretically investigated the evolution of these traits under LMC in the presence of inbreeding depression. When the reproductive group size evolves, the determination mechanism of sex ratio is important because the timescale of the sex ratio response to reproductive group size can affect the evolutionary process. We consider a spectrum of sex ratio determination mechanisms from purely unconditional to purely conditional, including intermediate modes with various relative strengths of unconditional and conditional effects. This analysis revealed that both the evolutionarily stable reproductive group size and ratio of males increase with higher inbreeding depression and with a larger relative strength of an unconditional effect in sex ratio determination. Unexpectedly, when the sex ratio is controlled purely conditionally, the reproductive group size cannot exceed three even under the severest level of inbreeding depression (i.e., lethal effect). The present study reveals the conditions for LMC to evolve through the analysis of the joint evolution of reproductive group size and sex ratio.     

Sex allocation and clutch size in parasitoid wasps that produce single-sex broods

The parasitoid wasp genus Achrysocharoides (Eulophidae) is unusual in that many of its species lay male and female eggs in single-sex clutches. The average clutch size of female broods is always greater than that of male broods, and in some species male clutch size is always one. We constructed models that predicted that severely egg-limited wasps should produce equal numbers of male and female eggs while severely host-limited wasps should produce equal numbers of male and female broods (and hence an overall female-biased sex ratio). Theory is developed to predict clutch size and sex ratio across the complete spectrum of host and egg limitation. A comparison of 19 surveys of clutch composition in seven species of Achrysocharoides showed a general pattern of equal numbers of male and female broods with a female-biased sex ratio (suggesting host limitation) although with considerable heterogeneity amongst collections and with a number of cases of unexpectedly low frequencies of male broods. Using a previous estimate of the relationship between fitness and size in the field, we predicted the maximally productive (Lack) clutch size for female broods of Achrysocharoides zwoelferi to be three. Of clutches observed in nature, 95% were equal to or smaller in size than the predicted Lack clutch size. When we manipulated local host density in the field, and as predicted by our models, clutch size and the proportion of female broods of A. zwoelferi decreased as hosts became more common, but the absolute frequency of male clutches was lower than expected. Copyright 1998 The Association for the Study of Animal Behaviour.     

The influence of developmental mortality on optimal sex allocation under local mate competition

In panmictic populations, optimal sex allocation is, under theassumptions of Fisher's model, not influenced by the probabilityof offspring developmental mortality, or by differences in mortalitybetween the sexes. In contrast, when mating opportunities areconfined to siblings, developmental mortality can influenceoptimal sex allocation. Many animal species have both localmating and developmental mortality. We show that when developmentalmortality is random for individual offspring, optimal sex allocationis influenced by mortality among males but not among females.Male mortality increases the allocation to males, but this shouldnever be male biased, even under extreme male mortality. Thisresult applies both when mothers are able to control the sexof individual offspring precisely, and when sex is allocatedwith binomial probability. The influence of mortality becomesprogressively larger when the variance of the distribution ofmortality over clutches diminishes. The reduction in fitnessis greater than the proportion of mortality, especially at smallclutch sizes, and mortality reduces the advantage of producingprecise sex ratios, and of local mate competition in general.     

Within-group aggression and the value of group members: theory and a field test with social wasps

We present a simple, general model of how the optimal levelof intra-group aggression should vary in different social contexts.A key component of this model is the value of the recipientof aggression to a potential aggressor (i.e., the ratio of expectedlong-term group productivity with the recipient present to theexpected group productivity with the recipient absent). Therecipient's value measures its contribution to group reproductivesuccess. We demonstrate theoretically that if aggression increasesthe aggressor's share of the group's expected total reproductiveoutput, but at the same time decreases the magnitude of thisoverall reproductive output, then the optimal level of aggressiontoward a recipient will decrease with increasing recipient'svalue. This proof establishes a rigorous theoretical connectionbetween the level of aggression within a group and the benefitsof belonging to such a group and can be tested by experimentallymanipulating the values of group members to each other. We test,and thus illustrate the utility of, this model by examiningaggression within experimentally-manipulated foundress associationsof social wasps. We show that the value of co-foundresses toeach other in the social wasp Polistes fuscatus lies in theirability to provide insurance against colony failure caused bythe loss of all tending foundresses. Removals of worker-destinedeggs and pupae, which increase the value of co-foundresses,both lead to significant reductions in aggression by the dominantfoundress, despite the fact that the immediate, selfish benefitsof competitive aggression should increase when empty brood cellsare present Removal of reproductive-destined eggs, which doesnot affect co-foundress value, but increases the benefits ofselfish aggression, causes a significant increase in aggressionby beta foundresses. Finally, wing reduction of subordinateco-foundresses significantly increases aggression by dominantfoundresses, as expected since the subordinate's value is reduced.Our results indicate that foundress aggression is sensitiveto the value of future cooperation, as predicted by the optimalaggression model. The model may apply widely to both invertebrateand vertebrate societies     

Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition

Hamilton's concept of local mate competition (LMC) is the standard model to explain female-biased sex ratios in solitary Hymenoptera. In social Hymenoptera, however, LMC has remained controversial, mainly because manipulation of sex allocation by workers in response to relatedness asymmetries is an additional powerful mechanism of female bias. Furthermore, the predominant mating systems in the social insects are thought to make LMC unlikely. Nevertheless, several species exist in which dispersal of males is limited and mating occurs in the nest. Some of these species, such as the ant Cardiocondyla obscurior, have evolved dimorphic males, with one morph being specialized for dispersal and the other for fighting with nest-mate males over access to females. Such life history, combining sociality and alternative reproductive tactics in males, provides a unique opportunity to test the power of LMC as a selective force leading to female-biased sex ratios in social Hymenoptera. We show that, in concordance with LMC predictions, an experimental increase in queen number leads to a shift in sex allocation in favour of non-dispersing males, but does not influence the proportion of disperser males. Furthermore, we can assign this change in sex allocation at the colony level to the queens and rule out worker manipulation.     

The heterozygosity theory of extra-pair mate choice in birds: a test and a cautionary note

Although extra-pair fertilizations (EPF) are common in socially monogamous systems, the benefits to females remain elusive. One potential benefit that recently has begun to receive empirical attention is increased offspring heterozygosity. We tested the heterozygosity hypothesis in the black-throated blue warbler Dendroica caerulescens using a panel of five microsatellite loci. We did not find any evidence that male heterozygosity influenced female extra-pair mating patterns, that females choose genetically dissimilar extra-pair mates, nor that extra-pair offspring were more heterozygous than within-pair offspring. However, simple Monte Carlo simulations indicated that the number of microsatellite loci used in this study, and most other recent studies, would detect an effect of heterozygosity only if that effect is pronounced. Thus, we were unable to demonstrate any effect of offspring heterozygosity in our study species, but a more subtle effect remains possible. Researchers wishing to test this hypothesis should use a large number of genetic markers and interpret negative results cautiously.     

Local mate competition with variable fecundity: dependence of offspring sex ratios on information utilization and mode of male production

Most models of local mate competition assume that the foundressescontributing offspring to a local mating group (‘patch’)all have the same fecundity. Frank (1985, 1987a, b), Herre (1985),and Yamaguchi (1985) consider models with variable fecundity,in which foundresses adjust their sex allocations in responseto the fecundities of the other foundresses in the patch. Herewe generalize and extend these models to include cases in whichfemales can respond to their own fecundities but not to eachother's (possibly because they must determine their sex allocationsbefore they arrive at the patch) and cases in which siblingsavoid mating with each other. Evolutionarily stable sex-allocationphenotypes are derived through both inclusive-fitness and population-geneticapproaches. Each model is solved for haploid, diploid, and haplodiploidgenetic systems with biparental and arrhenotokous modes of maleproduction. In models that allow sibmating, the biparental geneticsystems have one evolutionarily stable strategy (ESS) and thearrhenotokous systems have another, but within each of thesecategories, all three ploidys have the same ESS. Where femalescan respond only to their own fecundities, their brood sex Tratiosdecline with increasing brood size, but their absolute investmentsin males increase; this response occurs even where the meanpatch size is very large and the mean sex ratio of parentalinvestment is therefore indistinguishable from one-half. Patternsof sex allocation in many kinds of spatially structured populationsmay depend critically on the ways in which females perceiveand respond to environmental features that predict the fitnessdistributions of their local mating aggregations.     

Sex allocation theory reveals a hidden cost of neonicotinoid exposure in a parasitoid wasp

Sex allocation theory has proved to be one the most successful theories in evolutionary ecology. However, its role in more applied aspects of ecology has been limited. Here we show how sex allocation theory helps uncover an otherwise hidden cost of neonicotinoid exposure in the parasitoid wasp Nasonia vitripennis. Female N. vitripennis allocate the sex of their offspring in line with Local Mate Competition (LMC) theory. Neonicotinoids are an economically important class of insecticides, but their deployment remains controversial, with evidence linking them to the decline of beneficial species. We demonstrate for the first time to our knowledge, that neonicotinoids disrupt the crucial reproductive behaviour of facultative sex allocation at sub-lethal, field-relevant doses in N. vitripennis. The quantitative predictions we can make from LMC theory show that females exposed to neonicotinoids are less able to allocate sex optimally and that this failure imposes a significant fitness cost. Our work highlights that understanding the ecological consequences of neonicotinoid deployment requires not just measures of mortality or even fecundity reduction among non-target species, but also measures that capture broader fitness costs, in this case offspring sex allocation. Our work also highlights new avenues for exploring how females obtain information when allocating sex under LMC.     

Sex allocation and larval competition in a superparasitizing solitary egg parasitoid: competing strategies for an optimal sex ratio

1. Parasitic Hymenoptera reproduce by arrhenotokous parthenogenesis, and females of these species are able to control their progeny sex ratios. In structured populations of parasitic Hymenoptera, primary sex ratios are often highly biased toward females. However, sex ratio can be adjusted to the quality of encountered patches or hosts or be modified by differential developmental mortality.
2. In this paper, the effects were evaluated of the quality of encountered hosts and developmental mortality on the sex ratio in Anaphes victus , a solitary egg parasitoid whose first instar larvae present a sexual dimorphism and where superparasitism is regulated by larval fights between first instar larvae.
3. The results showed that a female-biased sex ratio is allocated to unparasitized hosts. In the presence of parasitized hosts, the second (superparasitizing) female produced a significantly higher sex ratio than the first female but the tertiary sex ratio (sex ratio at emergence) was not significantly different from the sex ratio produced with unparasitized hosts. The increase in the primary sex ratio produced by the second female was mostly compensated by the higher mortality of male larvae.