SEX-RATIO CONTROL IN A PARASITIC WASP,NASONIA VITRIPENNIS. II. EXPERIMENTAL ANALYSIS OF AN OPTIMAL SEX-RATIO MODEL

An optimal theory of facultative sex-ratio adjustment (Werren, 1980) was tested using the data from a series of sequential oviposition experiments (Orzack and Parker, 1986). Sex ratios produced by several genotypes in previously parasitized hosts differ significantly from the theoretical prediction. In addition, there is more variance of these “second” sex ratios than would be generated purely by sampling. I outline an alternative model of sex-ratio determination, based upon an imperfect ability of second females to detect previous parasitization, which accounts for the trends observed in the data. These results imply that selection on second sex ratios is weak or that females cannot control sex ratios finely enough to manifest the proper response. This analysis along with other results (Orzack and Parker, 1986; Parker and Orzack, 1985; Grant et al., 1974; Werren et al., 1981; Skinner, 1982) suggests that we need a more comprehensive theory of sex-ratio evolution, one which accounts for the diversity of first and second sex ratio phenotypes in this species.     

POLLEN PERFORMANCE AND SEX-RATIO EVOLUTION IN A DIOECIOUS PLANT

There has been a proliferation of studies, in a variety of taxa, that have detected sex-linked or cytoplasmic genes that enhance their own transmission via sex-ratio distortion. One of the most important parameters influencing the dynamics of these elements is the magnitude of their transmission advantage. In many systems, the mechanism of sex-ratio distortion is to abort X- or Y-bearing gametes. With this mechanism, the transmission advantage associated with sex-ratio distortion is diminished when the production of male gametes limits offspring production or when competition among the gametes of different males is intense. In this study, we analyzed the outcome of pollen competition between males that produced different sex ratios in the dioecious plant, Silene alba, and estimated how the sex-ratio bias influenced the transmission properties of the sex chromosomes. We varied the intensity of pollen competition by controlling the quantity of pollen used in crosses and used a combination of single-male pollinations and pollen mixtures to evaluate the effects of multiple paternity. Paternity in pollen mixtures was estimated using allozymes. Sex-ratio bias was directly influenced by the quantity of pollen, but the magnitude of this effect was small. The relative performance of pollen from different males varied substantially, especially when there was multiple paternity. Specifically, males with biased sex ratios sired far fewer offspring of either sex in pollen mixtures. In crosses involving single males, however, these “sex-ratio” males produced the same number of offspring as other males, so the female bias caused a significant transmission advantage for X-linked genes. X-linked genes could enhance their transmission via sex-ratio distortion in Silene populations, but the magnitude of this transmission advantage will depend on the ecological circumstances that influence the opportunity for multiple paternity.     

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.     

SUPPRESSION OF SEX-RATIO MEIOTIC DRIVE AND THE MAINTENANCE OF Y-CHROMOSOME POLYMORPHISM IN DROSOPHILA

Like several other species of Drosophila, D. quinaria is polymorphic for X-chromosome meiotic drive; matings involving males that carry a “sex-ratio” X chromosome (X^SR) result in the production of strongly female-biased offspring sex ratios (Jaenike 1996). A survey of isofemale lines of D. quinaria from several populations reveals that there is genetic variation for partial suppression of this meiotic drive. Crossing experiments show that there is Y-linked, and probably autosomal, variation for suppression of drive. Y-linked suppressors of X-chromosome drive have now been described in several species of Diptera. I develop a simple model for the maintenance of Y-chromosome polymorphism in species polymorphic for X-linked meiotic drive. One interesting feature of this model is that, if there is a stable Y-chromosome polymorphism, then the equilibrium frequency of the standard and sex-ratio X chromosomes is determined solely by Y-chromosome parameters, not by the fitness effects of the different X chromosomes on their carriers. This model suggests that Y-chromosome polymorphism may be easier to maintain than previously thought, and I hypothesize that karyotypic variation in Y chromosomes will be found to be associated with suppression of sex-ratio meiotic drive in other species of Drosophila.     

Sex-ratios of the wasp Nasonia vitripennis from self-versus conspecifically-parasitized hosts: local mate competition versus host quality models

Sex ratio patterns in the parasitoid wasp Nasonia vitripennis are frequently cited in support of a major group of evolutionary sex ratio models referred to as local mate competition (LMC) models. It has been shown repeatedly that, as predicted by LMC models, females generally oviposit a greater proportion of sons in previously parasitized hosts than in unparasitized hosts. However, this sex ratio pattern is also a prediction of another group of sex ratio models, the host quality models. Here I test a prediction of LMC models that is not also a prediction of host quality models: a female should produce a greater proportion of sons when she parasitizes a host previously parasitized by a conspecific female than when she parasitizes a host previously parasitized by herself. Females made this predicted distinction between self- and conspecifically-parasitized hosts under some conditions. There was no evidence that a female recognizes a self-parasitized host when her exposure to the host is interrupted by exposure to an unparasitized host, or that a female can distinguish between hosts parasitized by sisters versus nonsisters.     

SEX-RATIO MANIPULATION IN COLOR-BANDED POPULATIONS OF ZEBRA FINCHES

Significant correlations were found between attractiveness of leg-band color (determined by preference tests [Burley et al., 1982]) and sex ratio of offspring in two long-term breeding experiments involving zebra finches. In both experiments, birds with attractive band colors produced more same-sex offspring, while birds with unattractive band colors produced more opposite-sex offspring. The results of these experiments are consistent with those of a previous experiment (Burley, 1981). To explain the earlier results, I hypothesized that parents adjust their allocation to sons and daughters to produce offspring they “expect” to be most attractive. The purpose of such sex-ratio manipulation is to enhance fitness by the production of offspring with superior mate-getting opportunities. Two alternative hypotheses are presented here. One is that sex ratios change with parental age and/or experience. Evidence does not support this hypothesis. There were no temporal trends in sex ratio independent of band color. A second possibility is that sex ratios reflect differential parental ability to rear sons and daughters. This hypothesis cannot be conclusively tested on the basis of present evidence, but available evidence does not support it. Within color classes, weights of sons and daughters did not differ. Evidence indicates that parents effect secondary sex-ratio manipulation through the selective rejection of young, usually within six days of hatching. There is no evidence of manipulation prior to egg-laying. The costs associated with brood reduction probably set limits on the extent to which secondary manipulation can be profitably employed.     

CULTURAL INHERITANCE AS A MECHANISM FOR POPULATION SEX-RATIO BIAS IN REPTILES

Abstract.— Although natural populations of most species exhibit a 1:1 sex ratio, biased sex ratios are known to be associated with non‐Mendelian inheritance, as in sex‐linked meiotic drive and cytoplasmic inheritance (Charnov 1982; Hurst 1993). We show how cultural inheritance, another type of non‐Mendelian inheritance, can favor skewed primary sex ratios and propose that it may explain the female‐biased sex ratios commonly observed in reptiles with environmental sex determination (ESD). Like cytoplasmic elements, cultural traits can be inherited through one sex. This, in turn, favors skewing the primary sex allocation in favor of the transmitting sex. Female nest‐site philopatry is a sex‐specific, culturally inherited trait in many reptiles with ESD and highly female‐biased sex ratios. We propose that the association of nest‐site selection with ESD facilitates the maternal manipulation of offspring sex ratios toward females.     

Genetic Variation for Sex Ratio Traits within a Natural Population of a Parasitic Wasp, Nasonia Vitripennis

By analyzing isofemale strains extracted from a natural population of Nasonia vitripennis, we detected variation for the sex ratios produced in fresh hosts (first sex ratios) and in previously parasitized hosts (second sex ratios). Under simple assumptions of population structure, this between-strain heterogeneity of first sex ratios results in heterogeneity of fitnesses. There is approximately ten percent difference in average fitnesses between the strains. (The fitnesses of second sex ratios are analyzed in the accompanying paper.) Average first and average second sex ratios are uncorrelated. There is significant between-female heterogeneity within some strains for first sex ratios but not for second sex ratios. In addition, the average direct-developing and diapause first sex ratios (but not second sex ratios) are significantly correlated. There are significant correlations between the direct-developing and diapause sex ratios produced by the same female. The strains differ in their effects on the sex ratio and size of another female's brood in the same host. Data on these types of variation for sex ratio traits are essential for further progress in the study of sex ratio evolution.     

Effect of host density on offspring sex ratios and behavioral interactions between females in the parasitoid waspNasonia vitripennis (Hymenoptera: Pteromalidae)

Pairs of females of the parasitoid waspNasonia vitripennis were videotaped with one or two hosts. The presence of an additional host decreased the number of interactions between females but had no measured effect on the nature of the interactions, i.e., on whether the interaction involved physical contact or occurred while one of the females was parasitizing a host. The number of hosts did not itself affect offspring sex ratios but did influence which other factors were correlated with sex ratio. When there was one host, the proportion of sons was more positively correlated with utilization of previously drilled holes than with female-female interactions, whereas when there were two hosts, the reverse was true. Parasitizing an already parasitized host appeared to affect a female's sex ratio beyond any effects of the physical presence of another female: When two hosts were present, the proportion of sons was greater from hosts parasitized by both females than from hosts parasitized by only one female. The observation that parasitizations in previously drilled holes and female-female interactions are correlated with sex ratios is consistent with previous studies; however, that these relationships are host density dependent is a new result and remains unexplained.     

SEX-RATIO VARIATION IN THE GYNODIOECIOUS SHRUB HEBE STRICTISSIMA (SCROPHULARIACEAE)

The frequency of females was determined for eight populations of the gynodioecious shrub, Hebe strictissima (Scrophulariaceae) and related to plant vigor among populations, as indicated by the average number of leaves per shoot. The purpose was to test the idea that females should be more prevalent in relatively poor sites where plant vigor is low. This hypothesis was based on sex-ratio theory, coupled with the idea that fruit-set in the polleniferous morph (i.e., in “males”) is more dependent on vigor than it is in females. I found that, within populations, females produced significantly more fruit than males and that plant vigor did not differ significantly between the sexes. Fruit-set on males was positively and significantly correlated with the number of leaves per shoot within plants, among plants within populations, and among populations. No such correlations were found for females. The greater plasticity of the males altered the relative seed fitnesses of the two morphs among the eight populations, resulting in a negative correlation between female frequency and average plant vigor. I suggest, in general, that such plasticity may be an important factor in sex-ratio variation among populations and that it should be incorporated into models of sex-ratio evolution.     

Superparasitism and sex ratio in the solitary parasitoidEpidinocarsis lopezi

Highly variable sex ratios are found in the solitary parasitoidEpidinocarsis lopezi, both in the field and in a mass-rearing situation. Superparasitism is one of a number of factors which can influence sex ratios in parasitoid Hymenoptera. We show that superparasitism inE. lopezi is common in the field. Sex allocation decisions when parasitizing unparasitized hosts are not different from those with parasitized hosts; neither does differential mortality occur between the sexes in superparasitized hosts. Therefore superparasitism does not contribute to the variable sex ratio ofE. lopezi. Both the occurrence of superparasitism and the sex produced when ovipositing are shown to be functional forE. lopezi.     

Sex ratios under asymmetrical local mate competition: theory and a test with parasitoid wasps

Sex ratio theory allows unparalleled opportunities for testing how well animal behavior can be predicted by evolutionary theory. For example, Hamilton's theory of local mate competition (LMC) is well understood and can explain variation in sex allocation across numerous species. This allows more specific predictions to be developed and tested. Here we extend LMC theory to a situation that will be common in a range of species: asymmetrical LMC. Asymmetrical LMC occurs when females lay eggs on a patch asynchronously and male offspring do not disperse, leading to relatively weaker LMC for males emerging from later broods. Varying levels of LMC then lead to varying optimal sex ratios for females, depending on when and where they oviposit. We confirm the assumptions of our theory using the wasp Nasonia vitripennis and then test our predictions. We show that females adjust their offspring sex ratios in the directions predicted, laying different sex ratios on different hosts within a patch. Specifically, there was a less female-biased sex ratio when ovipositing on an unparasitized host if another host on the patch had previously been parasitized and a less female-biased sex ratio on parasitized hosts if females also oviposited on an unparasitized host.     

SEX-RATIO AND REPRODUCTIVE VARIATION IN THE MISTLETOE PHORADENDRON JUNIPERINUM (VISCACEAE)

Despite the fact that many parasitic and hemiparasitic plant species such as mistletoes are dioecious and occur in both the new and the old world, few data exist on variation in the sex ratio and allocation to reproduction in these taxa. We investigated 1) the sex-ratio of the xylem-tapping mistletoe Phoradendron juniperinum in relation to its age and position within the canopy of its host tree Juniperus osteosperma, and 2) reproductive effort in relation to the gender and age of mistletoe plants. Our surveys showed that P. juniperinum has a male-biased sex ratio. Despite this predominance of male individuals, females lived longer and had a greater reproductive effort than did males. A statistical analysis of the age distribution data indicated that the peak in the frequency of reproductively mature individuals was later in females than in males. These gender-specific distributions may have resulted 1) from sequential hermaphroditism (age-specific sex switching), or 2) because the average age of peak reproduction is later in female individuals. Because sex is genetically determined in a closely related genus of mistletoe and because we have no data to indicate sex switching in this species, we feel that our data support the interpretation that female individuals, on average, show a peak in reproductive vigor at an older age relative to males. While delayed reproduction in females may be favored because reproductive effort and success appear to be age-dependent in females of this species, both sexes can become reproductively mature relatively early in life. Further, because 1) allocation to reproduction as a function of age increases more rapidly for females of this species relative to males, and 2) because there may be a higher resource cost associated with reproduction in females, we hypothesized that female individuals would be more abundant in the best quality locations within the host tree so as to maximize the opportunity to meet those costs. In spite of the association between gender and some host characteristics, there was no indication that female plants were located in sites most favorable to either their carbon or water balance. We discuss reasons why this may be the case.     

SEX-RATIO MANIPULATION IN RESPONSE TO HOST SIZE BY THE PARASITOID WASP SPALANGIA CAMERONI: A LABORATORY STUDY

The prediction of Charnov et al.'s (1981) host-size model that there should be a negative relationship between host size and wasp sex ratio (proportion sons) was supported for Spalangia cameroni, a solitary parasitoid wasp. The relationship was shown to be a result of offspring sex manipulation by females in response to host size rather than a result of differential mortality of the sexes. A major assumption of the host-size model is that host size has a greater effect on the ultimate reproductive success of emerging female wasps than of males. This assumption was not supported. Host size had a positive effect on the size of both male and female S. cameroni. However, neither host size nor wasp size affected longevity, production of offspring by females, or ability of males to compete for mates. Host size may differentially affect the reproductive success of female and male wasps through effects on other aspects of reproductive success. Tests of the assumptions of offspring sex-ratio manipulation hypotheses are scarce but critical, not only for parasitoid wasps, but also for other organisms.     

Intraspecific host discrimination and larval competition inMicroplitis croceipes,Microplitis demolitor,Cotesia kazak (HYM.: Braconidae) andHyposoter didymator HYM: Ichneumonidae), parasitoids ofHeliothis virescens (LEP.: Noctuidae)

Intraspecific host discrimination and larval competition were studied forMicroplitis croceipes (Cresson),Microplitis demolitor Wilkinson,Cotesia kazak (Telenga), andHyposoter didymator (Thunberg), solitary endoparasitoids of the tobacco budworm,Heliothis virescens (F.). In ovipositional choice tests between unparasitized and parasitized hosts, the mean number of ovipositions for unparasitized hosts was significantly higher than the mean number of ovipositions for hosts parasitized once by a conspecific female forC. kazak andH. didymator, demonstrating that females of these two species discriminate against hosts recently (within a few seconds) parasitized by a conspecific female. No significant difference in oviposition occurred between these two kinds of hosts forM. croceipes andM. demolitor. Mean percent parasitization by a second conspecific female was determined at 24, 48, and 72 h delays in time between the first and second female attack, and with no delay. Except for the 0 h time delay forC. kazak andH. didymator, percent parasitization by a second conspecific female generally decreased as the delay in time between the first and second female attack increased. When the second parasitization immediately followed the first, one parasitoid larva always eliminated the other by physical combat. With a 24 or 48 h delay between the first and second parasitization, the younger larva was the victor over the older larva forM. croceipes, M. demolitor andC. kazak in at least 50% of the cases. Elimination of older larvae by younger larva was by physical attack. However, forH. didymator, the older instar was the victor, and elimination of younger larvae by older larvae was probably through physiological processes. Further, older larvae ofH. didymator apparently killed the eggs of the second female by physiological processes.      

Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp

Most parasitoid female wasps can distinguish between unparasitized and parasitized hosts and use this information to optimize their progeny and sex allocation. In this study, we explored the impact of mating on oviposition behaviour (parasitism and self‐ and conspecific superparasitism) on both unparasitized and already parasitized hosts in the solitary parasitoid wasp Eupelmus vuilleti (Crw.) (Hymenoptera: Eupelmidae). Virgin and mated females had the same oviposition behaviour and laid eggs preferentially on unparasitized hosts. The sex ratio (as the proportion of females) of eggs laid by mated females in parasitism and conspecific superparasitism was 0.67 ± 0.04 and 0.57 ± 0.09, respectively. Likewise, females laid more eggs in conspecific superparasitism than self‐superparasitism under our experimental conditions. These experiments demonstrate that E. vuilleti females can (i) discriminate between unparasitized and parasitized hosts and adapt the number of eggs they lay accordingly, and (ii) probably discriminate self from conspecific superparasitized hosts. Finally, mating does not appear to influence the host discrimination capacity, the ovarian function, or the oviposition behaviour.     

Presence of a conspecific increases superparasitism but not infanticide under self‐ and conspecific superparasitism in a semisolitary parasitoid,Echthrodelphax fairchildii (Hymenoptera: Dryinidae)

Female parasitoids are expected to avoid superparasitism (ovipositing in and/or on parasitized hosts) when unparasitized hosts are available. However, when the supply of unparasitized hosts is restricted, they are expected to self‐ as well as conspecifically superparasitize. One of the cues of a reduced availability of unparasitized hosts is the presence of a conspecific. Moreover, if the focal species can perform infanticide, after encountering a conspecific female, the females are expected to kill eggs existing in and/or on hosts when superparasitizing, because the eggs are more likely to be laid by others. In this study we investigated whether females of an infanticidal semisolitary parasitoid, Echthrodelphax fairchildii, increase their frequencies of superparasitism and infanticide after encountering a conspecific female. Echthrodelphax fairchildii females are capable of discriminating between self‐ and conspecific superparasitism until up to 0.75 h after the first egg was laid (self‐superparasitism frequency < conspecific superparasitism frequency). As expected, the female parasitoids were more likely to perform self‐ and conspecific superparasitism after they had encountered a conspecific. In particular, the self‐superparasitism frequency increased highly within a short period after the first oviposition, so that no difference between the self‐ and conspecific superparasitism frequencies was found. In contrast, the infanticidal‐probing frequency remained extremely low, irrespective of whether or not the female parasitoids had encountered a conspecific. Moreover, when superparasitizing, females usually laid female eggs. Possible causes for the low frequency of infanticidal probing and the female‐biased sex ratio are discussed.     

SEX-RATIO SELECTION IN A BIVOLTINE THRIPS. I. CONDITIONAL SEX-RATIO MANIPULATION AND FITNESS VARIATION

Females of the bivoltine thrips Elaphrothrips tuberculatus (Hood) (Insecta: Thysanoptera) produce broods of either all males (by viviparity) or all females (by oviparity). Measurements of the sex-allocation ratio, ecological and physiological conditions affecting male and female offspring body size, and correlates of the relative fitnesses of adult males and females in relation to size indicate that female parents tend to be viviparous (produce males) if their offspring will become relatively large adults, and that males gain more in fitness from large size than do females. However, the conditions that link sex allocation with offspring fitness differ between the spring and summer generations. In spring, when breeding is synchronous, 1) oviparous and viviparous females do not differ in body size, 2) females tend to be viviparous where the fungus upon which they feed is relatively dense and where their offspring will become relatively large adults, and 3) fungus density is highly correlated with male and female offspring size. In summer, when breeding is relatively asynchronous, 1) viviparous females are much larger than oviparous females early (but not late) in the season, 2) large viviparous females begin breeding earlier than smaller ones, 3) offspring developing earlier in the season become larger adults, and 4) a higher proportion of females are viviparous earlier than later. Field experiments and field collections show that the covariation among sex allocation, conditions, and fitness is not caused by differential mortality by size or sex. Differences between the spring and summer generations in the cues used by females to adjust offspring sex ratio may be caused by seasonal variation in the factors that affect offspring size. However, in both generations, females tend to produce sons only when their offspring will become relatively large adults, whereas daughters are produced regardless of offspring size. These data suggest that females of E. tuberculatus avoid production of males (the sex with higher variance in expected fitness) when the size of their offspring is relatively uncertain.     

A sex ratio theory of gregarious parasitoids

Summary A mathematical model is constructed to explain a density-dependent increase in the progeny sex ratios of gregarious parasitoids. In the model we considered non-cooperative game between females concerned with their own inclusive fitness. Equilibrium progeny sex ratios of the first and second females ovipositing on the same host are expressed in terms of the probability of double parasitism (p), the ratio of a male to a female in contribution to resource competition (α), the clutch size ratio between the two females (β), the crowding effect on female reproductive success (γ), and the inbreeding coefficient (f). Major predictions from the model are: 1) the progeny sex ratios of both the first and second females increase withp, 2) as β becomes smaller, the progeny sex ratios of the first females decrease, while those of the second females dramatically increases, 3) when a host is attacked by at most two wasps, the sex ratio of the total number of eggs laid on the host does not exceed 0.25. The effects of α and preferential death by female progeny in doubly parasitized hosts are considered as factors responsible for an excess number of males at emergence. Some possible modes of density-dependent increase in the sex ratios of the overall progeny populations is also discussed on the basis of the present model.     

Sex ratios when helpers stay at the nest

This study investigates the evolution of the sex ratio (parental investment in sons) when breeding adults are supported by help provided by nonbreeding individuals of one sex. The study also assumes that the helping sex remains on its natal site to compete for the opportunity to breed, whereas the nonhelping sex disperses. Two kin-selection models are presented, both of which incorporate the age structure found in many natural populations where such helping occurs. The first model assumes that helpers increase the survival of their parents. The second model assumes that helpers are indiscriminant: a helper chooses to increase the survival of a random pair of adults breeding on its natal patch. In both models, sex ratios are not always biased toward the sex that provides the most help. When helpers do not discriminate (second model), the direction of sex-ratio bias is determined solely by the size of the benefit of helping behavior. When this benefit is small, sex-ratio evolution is primarily influenced by local resource competition and sex ratios are biased toward the nonhelping (dispersive) sex. If the benefit of help is large enough, the effect of local resource competition is reduced and sex-ratio bias favors the helpful sex. When helpers help only their parents, the same qualitative relationship exists between the direction of sex-ratio bias and the benefit of helping. In this case, however, the direction of sex-ratio bias is also influenced by the size of the social group, mortality, and which individual (mother or father) controls the sex ratio. This study also investigates a sex-ratio conflict that exists between mates. Helping behavior of nonbreeders can act to alleviate the disparities between the optimal sex ratio from the perspective of a mother and that from the perspective of a father. This consequence of helping has not been previously recognized.