Oviposition behavior and progeny allocation of the polyembryonic waspCopidosoma floridanum (Hymenoptera: Encyrtidae)

Oviposition behavior was used to determine the primary clutch size and sex ratio of the polyembryonic wasp Copidosoma floridanumAshmead (Hymenoptera: Encyrtidae) parasitizing Pseudoplusia includens(Walker) (Lepidoptera: Noctuidae). The laying of a female egg was associated with a pause in abdominal contractions during oviposition, while the laying of a male egg was associated with uninterrupted abdominal contractions. Although unmated females produced only male broods, they also displayed male and female egg oviposition movements. Wasps always laid a primary clutch of one or two eggs. For mated females if only one egg was laid, the emerging secondary clutch was all male or female, but if two eggs were laid a mixed brood of males and females was almost always produced. The secondary clutch of single sex broods was usually between 1000 and 1200 individuals, but the secondary clutch of mixed broods averaged 1143 females and 49 males. Thus, the primary sex ratio for mixed broods was 0.5 (frequency males), but the secondary sex ratio was 0.042. Manipulation of the sequence of male and female egg oviposition or of the primary clutch did not produce major alterations in the secondary clutch size or sex ratio.     

Egg load is a cue for offspring sex ratio adjustment in a fig‐pollinating wasp with male‐eggs‐first sex allocation

Fig‐pollinating wasps (Agaonidae) only reproduce within fig tree inflorescences (figs). Agaonid offspring sex ratios are usually female‐biased and often concur with local mate competition theory (LMC). LMC predicts less female‐bias when several foundresses reproduce in a fig due to reduced relatedness among intra‐sexually competing male offspring. Clutch size, the offspring produced by each foundress, is a strong predictor of agaonid sex ratios and correlates negatively with foundress number. However, clutch size variation can result from several processes including egg load (eggs within a foundress), competition among foundresses and oviposition site limitation, each of which can be used as a sex allocation cue. We introduced into individual Ficus racemosa figs single Ceratosolen fusciceps foundresses and allowed each to oviposit from zero to five hours thus variably reducing their eggs‐loads and then introduced each wasp individually into a second fig. Offspring sex ratio (proportion males) in second figs correlated negatively with clutch size, with males produced even in very small clutches. Ceratosolen fusciceps lay mainly male eggs first and then female eggs. Our results demonstrate that foundresses do not generally lay or attempt to lay a ‘fixed’ number of males, but do ‘reset to zero’ their sex allocation strategy on entering a second fig. With decreasing clutch size, gall failure increased, probably due to reduced pollen. We conclude that C. fusciceps foundresses can use their own egg loads as a cue to facultatively adjust their offspring sex ratios and that foundresses may also produce more ‘insurance’ males when they can predict increasing rates of offspring mortality.     

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.     

Pollinating fig wasp Ceratosolen solmsi adjusts the offspring sex ratio to other foundresses

Abstract Local mate competition theory predicts that offspring sex ratio in pollinating fig wasps is female‐biased when there is only one foundress, and increased foundress density results in increased offspring sex ratio. Information of other foundresses and clutch size have been suggested to be the main proximate explanations for sex ratio adjustment under local mate competition. Our focus was to show the mechanism of sex ratio adjustment in a pollinating fig wasp, Ceratosolen solmsi Mayr, an obligate pollinator of the functionally dioecious fig, Ficus hispida Linn., with controlled experiments in the field. First, we obtained offspring from one pollinator and offspring at different oviposition sequences, and found that offspring sex ratio decreased with clutch size, and pollinators produced most of their male offspring at the start of bouts, followed by mostly females. Second, we found that offspring sex ratio increased with foundress density, and pollinators did adjust their offspring sex ratio to other females in the oviposition patches. We suggest that when oviposition sites are not limited, pollinators will mainly adjust their offspring sex ratio to other foundresses independent of clutch size changes, whereas adjusting clutch size may be used to adjust sex ratio when oviposition sites are limited.     

TESTING MODELS OF FACULTATIVE SEX RATIO ADJUSTMENT IN THE POLLINATING FIG WASP PLATYSCAPA AWEKEI

Female hymenoptera are renowned for their ability to adjust offspring sex ratio to local mate competition. When two females share a patch, they frequently produce clutches that differ in size, the female with the larger clutch optimally producing a more female‐biased sex ratio and vice versa. Females can base their sex allocation on their own clutch size only (“self‐knowledge”) or on both females’ clutch sizes (“complete knowledge”). Few studies have genotyped offspring so that each mother's contribution can be considered separately while none has found that both sources of information are used simultaneously. We genotyped 2489 wasps from 28 figs and assigned their maternity to one of the two foundress females. We argue that likelihood is a very convenient method to compare alternative models, while fitness calculations help to appreciate the cost of maladaptation. We find that the pollinating fig wasp Platyscapa awekei simultaneously uses its own as well as the other females clutch size in allocating sex. Indeed, the complete knowledge model explains the data 36 times better than the self‐knowledge model. However, large clutches contained fewer males than the optimal predictions leading to a median selection coefficient of 0.01.     

The mechanism of sex ratio adjustment in a pollinating fig wasp

Sex ratio strategies in species subject to local mate competition (LMC), and in particular their fit to quantitative theoretical predictions, provide insight into constraints upon adaptation. Pollinating fig wasps are widely used in such studies because their ecology resembles theory assumptions, but the cues used by foundresses to assess potential LMC have not previously been determined. We show that Liporrhopalum tentacularis females (foundresses) use their clutch size as a cue. First, we make use of species ecology (foundresses lay multiple clutches, with second clutches smaller than first) to show that increases in sex ratio in multi-foundress figs occur only when foundresses are oviposition site limited, i.e. that there is no direct response to foundress density. Second, we introduce a novel technique to quantify foundress oviposition sequences and show, consistent with the theoretical predictions concerning clutch size-only strategies, that they produce mainly male offspring at the start of bouts, followed by mostly females interspersed by a few males. We then discuss the implications of our findings for our understanding of the limits of the ability of natural selection to produce 'perfect' organisms, and for our understanding of when different cue use patterns evolve.     

Quantitative tests of sex ratio models in a pollinating fig wasp

Pollinating fig wasps are often used to study sex ratio evolution in structured mating populations. Theory predicts a female-biased sex ratio, becoming less female biased as female (foundress) density increases. We usedLiporrhopalum tentacularis to test two mechanisms of sex ratio control when foundresses oviposit simultaneously: (1) foundresses facultatively adjust the number of males in clutches, and (2) they produce the same number of males regardless of clutch size, which, given limited numbers of oviposition sites, would lead to increases in sex ratio with increasing density. We then examined whether foundresses can oviposit sequentially into figs. When oviposition was simultaneous, brood composition indicated facultative adjustment, although sex ratios were more female biased than predicted. Instead, foundresses appeared to adjust their sex ratio in response to both others ovipositing and their own fecundity. We also found that foundresses are able to oviposit completely sequentially, with those arriving second adjusting their sex ratio in response to the previous oviposition. Hence, pollinating wasps may fail to fit the predictions of classical sex ratio theory because the conditions under which foundresses oviposit, and their responses to changes in such conditions, are more complex than once assumed. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Putting your eggs in several baskets: oviposition in a wasp that walks between several figs

The interaction between figs (Ficus spp., Moraceae) and their pollinator fig wasps (Hymenoptera: Agaonidae) is an obligate mutualism, but females of dioecious fig trees exploit fig wasps without providing rewards. Figs are closed inflorescences that typically trap pollinator females after entry, but some fig wasp species can re‐emerge (although wingless) and subsequently oviposit in and pollinate further figs. Using glasshouse populations, we examined the sex ratios and clutches laid by single foundresses of Kradibia tentacularis (Grandi) in their first and subsequent male figs of Ficus montana Blume, and how the probability of emergence and entering a second fig varied between seasons. A maximum of four figs were entered by any one foundress. Wingless foundresses were able to locate and enter figs up to 60 cm from the first fig they entered, but the probability of entry declined sharply with distance from that fig. The foundresses that re‐emerged produced slightly higher adult offspring totals than those that failed to re‐emerge. Clutch sizes of a single foundress in its first fig equalled those in all the subsequent figs combined, with clutch size per fig decreasing when more figs were entered. Smaller clutches had less female‐biased sex ratios. Figs were more numerous in summer than in winter, but the proportion of figs entered by only wingless foundresses remained unchanged. Movement between figs increases pollinator reproductive success in male figs, thereby encouraging foundresses that encounter a female tree to also move between and pollinate several female figs.     

Molecular markers reveal reproductive strategies of non‐pollinating fig wasps

1. Fig wasps have proved extremely useful study organisms for testing how reproductive decisions evolve in response to population structure. In particular, they provide textbook examples of how natural selection can favour female‐biased offspring sex ratios, lethal combat for mates and dimorphic mating strategies. 2. However, previous work has been challenged, because supposedly single species have been discovered to be a number of cryptic species. Consequently, new studies are required to determine population structure and reproductive decisions of individuals unambiguously assigned to species. 3. Microsatellites were used to determine species identity and reproductive patterns in three non‐pollinating Sycoscapter species associated with the same fig species. Foundress number was typically one to five and most figs contained more than one Sycoscapter species. Foundresses produced very small clutches of about one to four offspring, but one foundress may lay eggs in several figs. 4. Overall, the data were a poor match to theoretical predictions of solitary male clutches and gregarious clutches with n ? 1 females. However, sex ratios were male‐biased in solitary clutches and female‐biased in gregarious ones. 5. At the brood level (all wasps in a fig), a decrease in sex ratio with increasing brood size was only significant in one species, and sex ratio was unrelated to foundress number. In addition, figs with more foundresses contain more wasp offspring. 6. Finally, 10–22% of females developed in patches without males. As males are wingless, these females disperse unmated and are constrained to produce only sons from unfertilised eggs.     

Models of clutch size in insect oviposition

Models for clutch size in species where a female deposits eggs into a larval resource of limited carrying capacity are developed. Previous models of clutch size related mainly to vertebrates (notably birds) where parental care limits clutch size. Our models cover cases where a single female “saturates” a larval food patch with larvae. The main predictions are that (1) extra eggs should be laid to compensate for larval moratility; (2) clutches should generally be smaller than the size that yields the maximum number of surviving larvae/clutch; (3) in species that gain resources for eggs in the adult stage, clutch size will be unaffected by age-independent parental mortality between clutches; (4) clutch size should reduce throughout life in species that gain resources for eggs before the adult stage; (5) similar species, but which are constrained to produce constant-sized clutches, should lay smaller clutches if their total potential egg production is low; (6) clutch size should increase with increasing search costs for oviposition sites. An ESS model of double-oviposition (where two females sometimes lay in the same larval food patch) indicates that the first female should generally lay more eggs than the second female; the difference in clutch size should decrease as the probability of double-oviposition increases, and should decrease as the search costs for larval food plants decreases. Many of the predictions have some support from data on insect oviposition.     

Do Fig Wasps Produce Mixed Paternity Clutches?

Pollinating fig wasps (Hymenoptera, Agaonidae) have been the focus of numerous studies examining sex ratio evolution. Recently, molecular genetic techniques have been introduced that assume single matings in fig wasps, yet their mating biology has not been investigated genetically. We used recently developed microsatellite markers to investigate whether a pollinating fig wasp (Liporrhopalum tentacularis Grandi) produces single or mixed paternity clutches. The clutches of 12 females which had had the opportunity to mate with males of different genotypes were investigated. The results suggest that, at least in this species of fig wasp, single paternity clutches are the norm. Based on our behavioural observations, this appears to be due to mating with a single male rather than sperm competition.     

Sex allocation and clutch size in the gregarious larval endoparasitoid wasp, Cotesia glomerata

The ability of the gregarious larval endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) to adjust progeny sex ratio and clutch size was investigated. The sex ratios (proportion of males) of field clusters were diverse, but many (70%) were female-biased. Nearly 10% yielded males only, suggesting a low percentage of unmated females in the field. In over half of the clusters containing females, the sex ratio was below 0.3. Superparasitism was common in the field, and females were believed to increase progeny sex ratio when attacking previously-parasitized hosts. However, in a single oviposition bout, sex allocation was not precisely controlled both in the field and laboratory. In the laboratory, the number of eggs laid in a day tended to decrease with increasing female age. For females which were offered two hosts per day and for those offered three hosts per day, this value became nearly the same several days after the start of oviposition. The total number of hosts which a female could parasitize during her lifetime was often less than 40. Some of the old females which attacked more than 40 hosts produced male-biased clutches; this was due to sperm depletion, because sperm remained viable throughout a female's lifetime. The amount of sperm used in a single oviposition bout seemed fixed and was not dependent on the number of eggs laid. Females with much oviposition experience did not produce new eggs to compensate for deposited eggs, and the efficiency of egg use (deposited eggs/total eggs) was more than 80%.     

Effects of time-dependent competition for oviposition sites on clutch sizes and offspring sex ratios in a fig wasp

Fig wasps have been known as one of the best-documented examples of female-biased sex ratio predicted from the local mate competition (LMC) theory. However, observed sex ratios appear more female-biased than predicted. Before a close match between theory and observation can be claimed, the number and sex ratio of offspring left by each foundress in a multi-foundress syconium need to be determined. We examined the clutch size and sex ratio of individual females of the pollinator fig wasp Blastophaga nipponica (Agaonidae) in experiments using a pair of fertile and sterile females in which sequence and time interval of entering syconia were manipulated. To determine the number and sex ratio of offspring left by each foundress in a multi-foundress syconium, we prepared sterilized females that could oviposit ordinarily but whose offspring could not develop at all, by irradiating the females with ⁶⁰Co gamma rays. Female fig wasps contributed different numbers and sex ratios of offspring to the total brood within a syconium, due to different entry times among them. The variation in clutch sizes with different entry times appeared to be caused by competition for oviposition sites, and sex ratios to be adjusted according to the clutch size.     

Evolutionary stable sex ratios with non‐facultative male‐eggs first sex allocation in fig wasps

Sex allocation theory has long generated insights into the nature of natural selection. Classical models have elucidated causal phenomena such as local mate competition and inbreeding on the degree of female bias exhibited by various invertebrates. Typically, these models assume mothers facultatively adjust sex allocation using predictive cues of future offspring mating conditions. Here we relax this assumption by developing a sex allocation model for haplodiploid mothers experiencing local mate competition that lay a fixed number of male eggs first. Female egg number is determined by remaining oviposition sites or remaining eggs of the mother, depending on which is exhausted first. Our model includes parameters for variation in foundress number, patch size, fecundity and offspring mortality that allow us to generate secondary sex ratio predictions based on specific parameterizations for natural populations. Simulations show that: 1) in line with classical models, factors that increase sib‐mating result in mothers laying relatively more female eggs; 2) high offspring mortality leads to relatively more males as fertilization insurance; 3) unlike classical model predictions, sub‐optimal predictions, such as more males than females are possible. In addition, our model provides the first quantitative predictions for the expected number of males and females in a patch where typically only one mother utilizes a given patch. We parameterized the model with data obtained from seven species of southern African fig wasps to predict expected means and variances for numbers of male and female offspring for typical numbers of mothers utilizing a patch. These predictions were compared to secondary sex ratio data from single foundress patches, the most commonly encountered situation for these species. Our predictions matched both the observed number and variance of male and female offspring with a high degree of accuracy suggesting that facultative adjustment is not required to produce evolutionary stable sex ratios.     

Influence of egg size differences within egg clutches on larval parameters in nine libellulid species (Odonata)

Abstract.  1. In libellulids, egg size differs between species and populations. There are also size differences within egg clutches of individual females.
2. Past experiments suggest that there are two different types of egg clutches in libellulids. Egg size decreases significantly during oviposition in species that perform non-contact guarding during oviposition. In contrast, in species ovipositing in tandem, egg size is randomly distributed.
3. This study deals with the possible consequences of egg size variation within the different egg clutch types. The study examined whether there is a correlation between egg development time, offspring sex or larval size and egg size.
4. The current experiments were conducted in Namibia and Germany. Five non-contact guarding and four tandem guarding libellulid species were used.
5. In some species larger eggs needed more time to develop, in some species no correlation between egg size and egg development time could be found, whereas in other species larger eggs developed faster.
6. The sex ratio was biased towards females in Leucorrhinia dubia and in Sympetrum striolatum and egg size was not associated with gender.
7. In both egg clutch types larger eggs resulted in larger larvae. In this study, evidence was found that the effects of egg size diminished with progressing larval development under good conditions. However, it is possible that the effects may have a greater influence under harsh circumstances.     

Postemergence Experience Affects Sex Ratio Allocation in a Gregarious Insect Parasitoid

We tested the hypotheses that postemergence experience with plants (“early adult learning”) modifies sex ratio and clutch size allocations of Cotesia congregata (Say) (Hymenoptera: Braconidae), a gregarious larval endoparasitoid of Manduca sexta L. (Lepidoptera: Sphingidae). Emerging wasps were exposed for 2–3 h to (a) one of two host plants (tomato or tobacco) or no plant, and (b) one of two novel plants (arugula or parsley) or no plant. Each female was permitted a single oviposition in a host offered with one of the two plant species 24 h later. Hosts were reared on laboratory diet before and after parasitization. Wasps exposed to either host plant allocated proportionately more females to hosts offered with the plant species experienced at emergence than wasps with the alternate species, but clutch sizes did not differ. Irrespective of plant species, wasps exposed to novel plants allocated proportionately more females to hosts than wasps without plant experience, and larger clutches to hosts offered with parsley than with arugula. Differential responses to host and novel plants suggest inherent recognition of host foodplants by C. congregata. Results demonstrate a direct effect of learning on reproductive potential.     

Sex allocation and effects of superparasitism on secondary sex ratios in the gregarious parasitoid, Trichogramma chilonis (Hymenoptera: Trichogrammatidae)

The role of sex-controlling behaviour at oviposition in generating primary sex ratios, and the effect of larval competition on secondary sex ratios, were studied in the gregarious endoparasitoid, Trichogramma chilonis. The production of a fertilized (female) egg is indicated by the incorporation of a pause in abdominal movements during oviposition, while the absence of it indicates the production of an unfertilized (male) egg. During each ovipositional bout, the first male egg is deposited at the second oviposition, and thereafter at intervals of about eight eggs. This simple pattern enables the wasps to adjust their progeny sex ratios under local male competition to a wide range of host size. Inexperienced wasps do not distinguish between parasitized and healthy hosts. Immature mortality is not significantly different between the sexes when a host is attacked by a single wasp, while females suffer higher immature mortality than males when superparasitism occurs.     

Allocation of offspring size and sex by female black ratsnakes

How females allocate resources to each offspring and how they allocate the sex of their offspring are two powerful potential avenues by which mothers can affect offspring fitness. Previous research has focussed extensively on mean offspring size, with much less attention given to variance in offspring size. Here we focussed on variation in offspring size in black ratsnakes, Elaphe obsoleta . We collected and hatched 105 clutches (1283 eggs) over 9 years. We predicted that females should lay larger eggs, or more variable eggs, when the environment is less predictable. We also predicted that females laying early or laying larger eggs should produce mostly sons because adult males are larger than adult female ratsnakes. The largest hatchling was more than twice the length and almost four times the mass of the smallest hatchling. Variation in offspring size was itself highly variable, with CVs in offspring mass among clutches ranging from 1% to 25%. With one exception, the variables we expected should influence variation in offspring size had little effect. We found that clutch size increased with maternal size and that egg size decreased with clutch size, but we found no evidence that variance in egg size among clutches increased as the season progressed or that females increased the mean size of their offspring the later in the season they laid their eggs. Females in better condition after they finish laying their eggs did produce larger eggs. There was no relationship between within-clutch variation in egg size and laying date or mean egg size. Finally, sex ratio did not vary with mean egg size or hatching date. Given evidence that offspring size in snakes affects survival, selection should reduce variation in offspring size unless that variance enhances maternal fitness and yet we found little support for hypothesized advantages of varying offspring size.     

Subtle manipulation of egg sex ratio in birds

Mothers are predicted to overproduce male or female eggs when the relative fitness gains from one sex are higher and outweigh the costs of manipulation. However, in birds such biases are often difficult to distinguish from differential embryo or chick mortality. Using a molecular technique to identify the sex of early embryos, we aim to determine the effect of maternal nutrition on zebra finch (Taeniopygia guttata) egg sex ratios after 2 days of incubation, which is as close to conception as is currently possible. We found no overall bias in the sex ratio of eggs laid and sex did not differ with relative laying order under any diet regime. However, mothers on a low-quality diet did produce a female bias in small clutches and a slight male bias in large clutches. On a high-quality diet, mothers produced a male bias in small clutches and a female bias in large clutches. Those on a standard diet produced a roughly even sex ratio, irrespective of clutch size. These observed biases in egg sex are partly in line with predictions that, in this species, daughters suffer disproportionately from poor rearing conditions. Thus, when relatively malnourished, mothers should only rear daughters in small broods and vice versa. Sex-ratio patterns in this species therefore appear to be subtle.     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.