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.     

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.     

Brood parasitism and cooperative nesting in the moorhen,Gallinula chloropus

Summary During a two year study of the moorhen, Gallinula chloropus, a quarter of the nests found had two or more females laying in them. This was the result of two features of the moorhens' breeding biology: (1) Cooperative nesting; two (or more) females were paired to the same male. Both laid in the same nest, the second laid a large clutch synchronously to the first, and both cooperated in parental care. (2) Intraspecific brood parasitism; some females (parasites or dumpers) laid a small number of eggs at random in the nests' of neighbours. Cooperatively nesting females were mother and daughter, while parasite and host were not. Parasitic females laid in their own nest as well, and generally did so after completing a dumping sequence. Parasitic eggs were laid at random during the host's laying and incubation period, and were about a quarter as likely to produce an independent chick as were non-parasitic eggs. Parasitic females would probably have reared more chicks by laying in their own nests straight away, instead of dumping any eggs at all, because there was a strong decline in reproductive success with season. Possible reasons why they did not do so are discussed. Parasitised pairs tended to rear fewer own chicks than non-parasitised pairs. There was no evidence that hosts selectively destroyed parasitic eggs. Four hypotheses that explain why hosts accepted dumped eggs are considered. (1) The host pair were unaware of the dump, (2) the host male had copulated with the dumping female, (3) the dumper was related to one of the host pair, and (4) there was a benefit to the host pair because they gained extra helpers. These hypotheses were not supported by the data, but further tests are needed. As the cost of desertion was greater than the cost of acceptance of parasitic eggs, hosts may have been forced to accept.     

Maternal effects on begging behaviour: an experimental demonstration of the effects of laying sequence, hatch order, nestling sex and brood size

Differential resource allocation by females across the laying sequence has been hypothesised as a mechanism through which females could either compensate nestlings that hatch last in asynchronous broods or promote brood reduction. In this study we artificially incubated eggs and cross-fostered offspring to manipulate nestlings’ position in the hatching order, to identify whether the competitive ability of nestlings is dependent on position in the laying sequence. In both control and experimentally reversed broods, first hatched chicks had a higher survival than last hatched siblings. Yet, nestlings that hatched from eggs laid in the second half of a clutch begged with a greater intensity than nestlings hatched from eggs laid in the first half of a clutch. In natural broods, the greater begging competitiveness of nestlings from later-laid eggs led to a moderation of sibling competition and these nestlings achieved the same body size and weight as nestlings from eggs laid in the first half of the clutch. The lack of a substantial difference in the size and condition of surviving nestlings in respect to laying order suggests that differential resource allocation across the egg-laying sequence partially compensates for hatching last in asynchronous broods and reduces the negative effects of the nestling size hierarchy. The effect of laying order, brood size and experimental treatment also differed for male and female nestlings. Our study highlights the need to be aware of the complex and subtle effects of nestling sex and laying sequence when investigating genetic and environmental influences on individual fitness.     

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.     

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     

Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus)

Empirical evidence is growing that the offspring sex ratio in birds can be biased in relation to the body condition of parents during breeding. The sex ratio bias may come about because (1) the actual production of the two sexes may be skewed and/or (2) there may be a sex bias in early nestling mortality contingent on parental condition. By manipulating parental condition and giving them a control brood to rear, thereby eliminating effects operating via the eggs, we examined the extent to which parental condition influences the post-hatching survival of male and female lesser black-backed gulls, Larus fuscus. We found that the pre-fledging survival of male chicks was strongly reduced in all-male broods reared by parents in poor condition. Pre-fledging survival of female chicks was, however, unaffected by parental condition or brood sex composition. Thus, independently of any production biases, sex differences in nestling mortality alone can bias the offspring sex ratio at fledging in relation to the prevailing rearing conditions. In other studies on gulls we have, however, also shown that females in poor condition at laying preferentially produce female eggs. Clearly a bias in fledging sex ratio can occur within the same species due to a combination of differential production and differential post-laying mortality; the latter can involve a differential effect of poor egg quality on male and female offspring, differential effects of brood sex composition on their survival and a difference in the capacity of parents to rear males and females. All of these processes need to be taken into account in attempting to understand offspring sex ratios. Received: 15 February 2000 / Revised: 7 August 2000 / Accepted: 26 August 2000     

Precise sex ratio in a parasitic wasp: the result of counting eggs

Summary The parasitic wasp Nesolynx albiclavus maintains a very skewed offspring sex ratio (ca. 4% males). We studied proximate, causal factors of the son-daughter choice mechanism to obtain insight into the precision of the procedures and the underlying rules. We analyzed the number of males in clutches produced during sessions of 12 or 24 h. The results show that the timing of the next male egg depends on the time elapsed and the number of eggs laid since the previous one. The influence of the passage of time per se during non-laying periods was reduced in an experiment with 4-h periods. The data show that the first male egg is produced by a fairly rigid process: about the sixth egg in a run will be left unfertilized. No further male egg will appear in the next 10–20 eggs if they are laid in rapid succession.     

Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.     

Oviposition site selection and oviposition stimulation by conspecifics in the golden egg bug (<Emphasis Type="Italic">Phyllomorpha laciniata</Emphasis>): implications for female fitness

Phyllomorpha laciniata Vill. (Heteroptera, Coreidae) females lay eggs on the host plant and on the backs of conspecifics. Since egg survival is greater when eggs develop on the backs of conspecifics than when laid on plants, we predict that females should prefer to lay eggs on conspecifics. In addition, because conspecifics are a high-quality site that represents a limiting resource, females should experience oviposition stimulation upon an encounter with a conspecific. Our results reveal that, when both the host plant and conspecifics are available simultaneously, females lay eggs preferentially on conspecifics. The results also support the second prediction, since females housed with conspecifics lay more than twice the number of eggs than isolated females. Isolated females do not seem to retain eggs, suggesting that oviposition stimulation is the result of an acceleration of egg-maturation rates. Other studies have found oviposition stimulation by mating and have suggested that it is the result of male strategies to increase short-term male reproductive success at some cost to females. The evolutionary scenario of our model organism seems to be quite different since females benefit greatly from increasing egg laying when there are conspecifics, because the advantages in terms of offspring survival are likely to translate into substantial increases in female reproductive success.     

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.     

Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting

Parasitic female moorhens (Gallinula chloropus) lay from one to six eggs in the nests of conspecific neighbours. DNA fingerprinting was used to show that parasitic eggs could be correctly identified when they appeared in addition to or outside the host’s laying sequence. Moorhen hosts accept all parasitic eggs laid after the 2nd day of their laying period. To understand why moorhen hosts tolerate parasitic eggs, we tested two hypotheses. (1) The quasi-parasitism hypothesis: females lay their eggs in the evening when the host males are normally in attendance at the nest, so host males may allow parasitic females to lay in their nests in exchange for fertilizing their eggs. However, DNA fingerprinting showed that all the parasitic eggs were sired by the parasites’ mates. Parasitic moorhens frequently continue laying a clutch in their own nest, without a break in the laying sequence after a parasitic laying bout. The eggs laid by brood parasites in their own nests were also sired by their own mates. Therefore this hypothesis was rejected. (2) The kin selection hypothesis: if one or both members of the host pair are close relatives of the parasite, the costs of rearing parasitic chicks will be to some degree offset by inclusive fitness benefits. We examined the genetic relationships between parasites and their hosts using DNA fingerprinting and genealogical data. Natal philopatry by both sexes was relatively common in this population, and the probability that a neighbour of either sex was a first-order relative (parent-offspring) was calculated as 0.18. Although first-order relatives were not preferentially chosen as hosts over individuals that were not first-order relatives, even through random host selection there is almost a one-in-five chance that brood parasites in this population are closely related to their hosts. This may facilitate host tolerance of parasitic eggs. Other hypotheses are also discussed. Received: 3 February 1995/Accepted after revision: 27 August 1995     

Adoption or infanticide: options of replacement males in the European starling

The behaviour of a male bird towards a potential mate and her clutch may depend both on his expected paternity and on the likelihood that she will produce a replacement clutch if he commits infanticide. In this study we evaluate the choices made by replacement male European starlings Sturnus vulgaris. By removing males before and during laying, we induced other males, mainly neighbours, to mate with the reproductively active females. When the original male was removed before laying, a new male adopted the subsequent clutch in 14 out of 15 cases. When ten females were widowed during their laying period, replacement males never adopted their clutches. The paternity of replacement males was a function of when they replaced the former male. When replacement occurred more than 3 days before egglaying, the new male fathered nearly all offspring; when it occurred the day before laying, the new male still fathered more than every second young. When the original male was removed during his mate’s laying period, in five out of ten cases a replacement male committed infanticide by throwing out the eggs, but this only occurred in one out of 15 cases when removal took place before laying. The evidence for infanticide actually being committed by the replacement male was circumstantial. Four out of six of the females affected by apparent infanticide produced replacement clutches in which the male presumably had higher paternity than in the original clutch. In all cases, the male adopted the replacement clutch. In five cases when the original male was removed during laying, the neighbours neither adopted the brood nor committed infanticide, although they sometimes were seen courting the widowed female and copulating with her. These cases occurred later during laying than those were males comitted infanticide. The time from infanticide to the laying of the replacement clutch tended to increase as infanticide was committed later in the laying sequence. We conclude that strategies of potential replacement males are influenced by their expected paternity in the current brood and the probability that the female will produce an early replacement clutch. Received: 10 March 1995 / Accepted after revision: 28 October 1995     

Superparasitism and ovicide in parasitic Hymenoptera: theory and a case study of the ectoparasitoid Bracon hebetor

Summary Among insect parasitoids, superparasitism is said to occur when a second clutch of eggs is laid on a previously parasitized host. Ovicide occurs when a parasitoid destroys a clutch of eggs laid on a host by a previous female. Here, general models are constructed to predict the conditions which favor superparasitism and ovicide. Major predictions for the ovicidal model were that ovicide is more likely to occur if the time necessary to kill eggs is short, if travel times and the proportion of parasitized hosts increases and if the competitive advantage of a first clutch is large. The predictions of the models were tested by examining superparasitism and ovicide in Bracon hebetor (Say), a gregarious, ectoparasitoid of phytisiine moths. Using a wild and eye color mutant of B. hebetor to distinguish first and second clutches, it was found that the competitive advantage of a first clutch over a second clutch increased with the time between ovipositions. Patterns of superparasitism and ovicide in B. hebetor were in qualitative agreement with the major predictions of the model. Most notable, ovicide increased in frequency with a decrease in the overall rate of host encounter and an increase in the proportion of parasitized hosts encountered.     

Adaptive responses to local mate competition by the parasitoid,Telenomus remus

Summary The parasitic wasp, Telenomus remus, lays her eggs in diserete patches of moth eggs, where her offspring develop and mate before dispersal, satisfying conditions for local mate competition (LMC). In the presence of other ovipositing females, wasps lay a higher sex ratio (proportion males), as predicted by LMC theory, and achieve this by a combination of two mechanisms, (1) avoidance of superparasitism and a sequence of sex allocation initially biased towards males and (2) a direct increase in sex ratio in the presence of other wasps, sex ratio increases with the proportion of previously parasitized hosts, as predicted by LMC theory. In both cases, chemical traces left by foraging wasps are indicated as the stimuli causing wasps to increase the proportion of males allocated to hosts.     

Sex-specific effects of yolk-androgens on growth of nestling American kestrels

Maternally derived androgen hormones concentrate in avian egg yolks as the yolks grow on the female’s ovary, possibly forming a basis for important maternal effects in birds. In the American kestrel (Falco sparverius), experimental elevation of yolk androgens in the first-laid egg of a clutch (a-egg) to the concentrations found naturally in a clutch’s later-laid eggs reduces the growth rate of a-egg nestlings compared to controls. These findings, together with discoveries from other species that the effects of yolk androgens on growth of female nestlings may differ from their effects on growth of male nestlings, raise the hypothesis that natural changes in yolk-androgen concentrations with laying order are ultimately due to a difference between the sexes in their yolk-androgen sensitivity and between early- and late-laid eggs in their sex ratio. By re-analyzing previously published data and adding to the analysis data from previously unanalyzed blood samples used for sex determination, we investigated possible sex-specific effects of yolk-androgens in the context of a potential sex-biased laying order in free-living American kestrels. We used a multi-level, mixed model with a Gompertz function to analyze growth of nestlings hatching from a-eggs that were control-treated or in which we experimentally elevated yolk-androgen concentrations shortly after laying to the higher concentrations naturally found in later-laid eggs. We discovered that male nestlings were more susceptible than female nestlings to growth inhibition by yolk-androgen elevation but did not find a bias in sex ratio with respect to laying order. Together, these findings do not support the above hypothesis. However, they are consistent with the hypothesis that sex differences in yolk-androgen sensitivity enable mothers to economically tune reproductive effort to an individual offspring’s reproductive value, which can vary more for one sex than the other.     

Nestmate discrimination in social wasps: The role of exposure to nest and nestmates (Polistes fuscatus,Hymenoptera: Vespidae)

Summary In the laboratory, gynes (potential queens) of the paper wasp, Polistes fuscatus, exposed to both their natal nest and female nestmates (presumably their sisters) discriminate between female nestmates and unrelated females. However, gynes not exposed to their natal nest or conspecifics and gynes exposed only to female nestmates do not discriminate between female nestmates and unrelated females. Thus, the presence of the nest appears to be a requisite for the development of nestmate discrimination.     

Sexual dimorphism in house sparrow eggs

Recent evidence has revealed an apparently high degree of control by female birds over the physiological aspects of their reproduction and offspring sex allocation, consistent with adaptive hypotheses of sex allocation and differential investment in their offspring. In the house sparrow, we investigated possible mechanisms that may be used by females to enhance the fitness returns from a reproductive effort. Using molecular techniques, we demonstrate that house sparrow eggs containing male embryos are significantly larger than those containing female embryos. We also found that male embryos were laid randomly with respect to laying order. We speculate that this sexual dimorphism of eggs is adaptive, because male house sparrows show greater variance in condition-dependent reproductive success than females. More important, the result provides further evidence of the ability of females to detect or control ovulation of either male or female ova and to differentially invest in one sex over the other. Received: 19 January 2000 / Revised: 29 June 2000 / Accepted 20 July 2000     

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.     

Tactics of parasitic American coots: host choice and the pattern of egg dispersion among host nests

Summary I examined the tactics adopted by a conspecific brood parasite, the American coot (Fulica americana), and the degree to which these tactics reflect sources of mortality for parasitic eggs. Only 8% of parasitic eggs produced independent offspring, compared to a 35% success rate for non-parasitic eggs, and most mortality was due to egg-rejection by hosts or the consequences of laying eggs too late in the host's nesting cycle. Parasites usually laid parasitically before initiating their own nests and usually parasitized immediate neighbours. Parasites did not remove host eggs before laying their own egg, and egg disappearance in general was not more common at parasitized nests. I found no evidence for non-random host choice, either on the basis of stage of the host's nesting cycle or the host's brood size. The absence of adaptive host choice is likely a consequence of the fact that, due to host limitation, only a small proportion of parasites had meaningful variation among potential hosts to choose from. The pattern of egg dispersion among host nests by individual parasites appears to be a compromise between constraints imposed by host limitation and the increased success obtained from spreading eggs among nests. Most females laying fewer than five parasitic eggs laid them in a single host nest while females laying five or more eggs normally parasitized two or more hosts. An examination of egg rejection and survival rates showed that parasites would maximize success by laying a single egg per host nest, and the pattern of laying several eggs per host nest is likely a consequence of host limitation. However, no egg that was the fifth laid, or later, parasitic egg in a host nest was ever successful and this probably explains why most females laying five or more eggs parasitized more than one host.