Body size and the timing of egg production in parasitoid wasps

In insects several key fitness-related variables are positively correlated with intraspecific variation in body size, but little is known about size-related variation in the timing of egg production within species. Female insects are known to vary in the degree to which they concentrate egg production into the early part of life. This variation has been quantified as the ovigeny index, defined as the proportion of the maximum potential lifetime complement of eggs that is mature following emergence from the pupa. We tested the hypothesis that the timing of egg production depends both on body size and on host availability, by means of a dynamic programming model that predicted optimal resource allocation to reproduction and survival together with the resulting ovigeny index, in non-feeding synovigenic parasitoids of different sizes. As body size increases, the proportionate increase in resource allocation to initial egg load is less than the proportionate increase in allocation to lifetime fecundity and potential life span, leading to a deferred investment in reproduction as shown by a decrease in ovigeny index. High habitat quality and high habitat stochasticity in reproductive opportunities have a significant effect on the optimal allocation of resources to reproduction and survival, and thus select for early reproduction, i.e. an increased ovigeny index. The ovigeny concept – ovigeny index together with its life-history correlates – enables understanding of the general occurrence of size-related deferment of reproductive investment in parasitoid wasps and also helps explain a significant part of the considerable life-history variation found among such insects.     

Egg maturation strategy and survival trade-offs in holometabolous insects: a comparative approach

One of the key predictions of general life-history theory is that reproduction incurs a survival cost. Although there is a convincing body of evidence to support this prediction at the intraspecific level in insects, evidence at the interspecific level is relatively scarce, as is the case for other animals. By employing two methods of phylogenetically controlled analysis, we demonstrate the existence of a negative correlation between life-span and early life investment in reproduction, across a wide diversity of Lepidoptera. The measure of initial reproductive effort used was the 'ovigeny index', defined as the proportion of the lifetime potential egg complement that is mature (ready to lay) upon female emergence. We present a graphical model for holometabolous insects, illustrating the trade-offs that are hypothesized to occur among capital resources (soma vs non-soma and initial eggs vs storage) in relation to variation in ovigeny index. These trade-offs, for which there is some empirical support, are postulated to underlie the life-span/ovigeny index relationship observed in the Lepidoptera and also in other insect orders.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 293–302.     

Egg maturation, egg resorption and the costliness of transient egg limitation in insects

Although there is widespread agreement that the cost of oviposition underlies selective oviposition in insects, there is no consensus regarding which factors mediate the cost of oviposition. Models have suggested that egg costs are often paramount in those insects that do not continue to mature eggs during the adult stage (pro-ovigenic insects). Here we address the hypothesis that egg costs are generally less significant in synovigenic insects, which can replenish oocyte supplies through continuous egg maturation. A dynamic optimization model based on the biology of a highly synovigenic parasitoid, Aphytis aonidiae, suggests that the maximum rate of egg maturation is insufficient to balance the depletion of eggs when opportunities to oviposit are abundant. Transient egg limitation therefore occurs, which imposes opportunity costs on reproducing females. Thus, whereas the most fundamental constraint acting on the lifetime reproductive success of pro-ovigenic species is the fixed total number of eggs that they carry at eclosion, the most fundamental constraint acting on a synovigenic species is the maximum rate of oocyte maturation. Furthermore, the ability of synovigenic species to reverse the flow of nutrients from the soma to oocytes (i.e. egg resorption) has a dramatic influence on the cost of oviposition. Whereas females in hostrich environments may experience oviposition-mediated egg limitation, females in host-poor environments may experience oosorption-mediated egg limitation. Both forms of egg limitation are costly. Contrary to initial expectations, the flexibility of resource allocation that typifies synovigenic reproduction actually appears to broaden the range of conditions under which costly egg limitation occurs. Egg costs appear to be fundamental in mediating the trade-off between current and future reproduction, and therefore are an important factor favouring selective insect oviposition.     

Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera

Abstract. 1. Insects vary considerably between and within orders, and even within the same genus, in the degree to which the female's lifetime potential egg complement is mature when she emerges as an adult. 2. The ‘ovigeny index’ (OI) – the number of eggs females have ready to lay divided by the lifetime potential fecundity – quantifies variation in the degree of early life concentration of egg production, and also variation in initial reproductive effort. 3. Here, an integrated set of hypotheses is presented, based on a conceptual model of resource allocation and acquisition, concerning trade‐offs at the interspecific level between initial investment in egg production (as measured by OI) and other life‐history traits in holometabolous insects. 4. The evidence supporting each of these hypotheses is reviewed, and particular attention is paid to the Lepidoptera, as relevant life‐history data are rapidly accumulating for this ecologically and economically important group. 5. There is evidence at the interspecific level supporting: (i) a link between OI and a trade‐off between soma and non‐soma in Trichoptera and Hymenoptera (the proportionate allocation to soma decreases with increasing OI); (ii) a negative correlation between OI and dependency on external nutrient inputs (via adult feeding) in Hymenoptera and in Lepidoptera; (iii) a negative correlation between OI and the degree of polyandry (and nuptial gift, i.e. spermatophore, use) in Lepidoptera; (iv) negative correlations between OI and resource re‐allocation capabilities (egg and thoracic musculature resorption) in Hymenoptera and in Lepidoptera; (v) a negative correlation between lifespan and OI in Trichoptera, Hymenoptera, and Lepidoptera, indicating a cost of reproduction; (vi) a link between winglessness and an OI of one in Lepidoptera; (vii) a negative correlation between OI and the degree of female mobility in winged Lepidoptera; and (viii) a negative correlation between OI and larval diet breadth (as mediated by oviposition strategy) in Lepidoptera.     

Stochasticity in reproductive opportunity and the evolution of egg limitation in insects

Is reproduction by adult female insects limited by the finite time available to locate hosts (time limitation) or by the finite supply of eggs (egg limitation)? An influential model predicted that stochasticity in reproductive opportunity favors elevated fecundity, rendering egg limitation sufficiently rare that its importance would be greatly diminished. Here, I use models to explore how stochasticity shapes fecundity, the likelihood of egg limitation, and the ecological importance of egg limitation. The models make three predictions. First, whereas spatially stochastic environments favor increased fecundity, temporally stochastic environments favor increases, decreases, or intermediate maxima in fecundity, depending on egg costs. Second, even when spatially or temporally stochastic environments favor life histories with less‐frequent egg limitation, stochasticity still increases the proportion of all eggs laid in the population that is laid by females destined to become egg limited. This counterintuitive result is explained by noting that stochasticity concentrates reproduction in the hands of a few females that are likely to become egg limited. Third, spatially or temporally stochastic environments amplify the constraints imposed by time and eggs on total reproduction by the population. I conclude that both egg and time constraints are fundamental in shaping insect reproductive behavior and population dynamics in stochastic environments.     

Rate of nutrient allocation to egg production in a parasitic wasp

Recent years have seen a marked increase in our awareness of the need to incorporate greater physiological realism into studies of parasitoid behaviour and population dynamics. Quantification of the number of eggs produced as a result of a host-feeding event, the host-feeding gain, is essential for predicting when a parasitoid should bypass an opportunity for current reproduction (i.e. laying eggs) in order to feed from the host and, thus, increase its chances for future reproduction (i.e. producing further eggs). Using radioactively labelled amino acids, one of the main constituents of insect haemolymph, we followed the incorporation of a known quantity of nutrients into each individual egg laid over a long period of time relative to the average life span of the parasitoid. Although the maximum incorporation of nutrients obtained by the female from a discrete feeding event occurs within a short period of time, a large proportion of nutrients are stored and used gradually for egg production throughout the life of the parasitoid. We therefore provide novel experimental evidence showing that feeding gain is not a discrete event in time occurring shortly after feeding, as has so far been assumed, but is instead spread throughout the parasitoid''s lifetime. This has important consequences for calculating the increase in lifetime fitness as a result of a feeding event, a common currency of models that aim to predict feeding and oviposition behaviour in parasitoids.     

Individual quality and food availability determine yolk and egg mass and egg composition in tree swallows Tachycineta bicolor

Variation in egg size and composition can have important consequences for the quality of offspring. We investigated the factors influencing the yolk mass and egg mass of tree swallows breeding in Ithaca, NY. Using a nondestructive technique to estimate yolk mass via standardized digital-candler photographs, we compared yolk size and egg size of tree swallows Tachycineta bicolor in response to variation in food availability and individual quality. Insect availability one to three days prior to laying, but not four to six days, predicted yolk mass, while insect availability two to three days prior to laying predicted total egg mass. This suggests that, while eggs are formed over longer periods, food availability closer to time of laying has the greatest influence on egg size. These results were supported by collected eggs, as yolk rings revealed that tree swallow eggs are formed over 5–6 days. There was an influence of female quality as well, with early laying birds, independent of food availability, laying larger eggs. Eggs laid later in the laying sequence had larger yolks and greater egg mass. Overall, variation in egg quality appears to be due to a combination of environmental conditions, reflected in food resources, individual quality, and allocation tradeoffs during the laying period.     

Small body size in an insect shifts development, prior to adult eclosion, towards early reproduction

Life-history theory has suggested that individual body size can strongly affect the allocation of resources to reproduction and away from other traits such as survival. In many insects, adults eclose with a proportion of their potential lifetime egg production that is already mature (the ovigeny index). We establish for the solitary parasitoid wasp Aphaereta genevensis that the ovigeny index decreases with adult body size, despite both initial egg load and potential lifetime fecundity increasing with body size. This outcome is predicted by adaptive models and is the first unequivocal intraspecific demonstration. Evidence suggests that a high ovigeny index carries a cost of reduced longevity in insects. Our results therefore contribute to the emerging evidence that small body size can favour a developmental shift in juveniles that favours early reproduction, but which has adverse late-life consequences. These findings are likely to have important implications for developmental biologists and population biologists.     

Fitness conflicts and the costs of sociality in communal egg layers: a theoretical model and empirical tests

Individuals within complex social groups often experience reduced reproduction owing to coercive or suppressive actions of other group members. However, the nature of social and ecological environments that favour individual acceptance of such costs of sociality is not well understood. Taxa with short periods of direct social interaction, such as some communal egg layers, are interesting models for study of the cost of social interaction because opportunities to control reproduction of others are limited to brief periods of reproduction. To understand the conditions under which communal egg layers are in fitness conflict and thus likely to influence each other's reproduction, we develop an optimality model involving a brood guarding 'host' and a nonguarding disperser, or 'egg dumper'. The model shows that when, where intermediate-sized broods have highest survival, lifetime inclusive fitnesses of hosts and dumpers are often optimized with different numbers of dumped eggs. We hypothesize that resolution of this conflict may involve attempts by one party to manipulate the other's reproduction. To test model predictions we used a lace bug (Heteroptera: Tingidae) that shows both hosts and egg dumpers as well as increased offspring survival in response to communal egg laying. We found that egg-dumping lace bugs oviposit a number of eggs that very closely matches predicted fitness optimum for hosts rather than predicted optimum of dumpers. This result suggests that dumpers pay a social cost for communal egg laying, a cost that may occur through host suppression of dumper reproduction. Although dumper allocation of eggs is thus sub-optimal for dumpers, previous models show that the decision to egg dump is nevertheless evolutionarily stable, possibly because hosts permit just enough dumper oviposition to encourage commitment to the behaviour.     

Time limitation, egg limitation, the cost of oviposition, and lifetime reproduction by an insect in nature

For more than 80 years, ecologists have debated whether reproduction by female insect herbivores and parasitoids is constrained by the time needed to find hosts (time limitation) or by the finite supply of mature eggs (egg limitation). Here we present the first direct measures of permanent time limitation and egg limitation and their influences on the cost of oviposition and lifetime reproduction for an insect in nature. We studied the gall midge Rhopalomyia californica, which neither matures nor resorbs eggs during the adult stage. By sampling females soon after their death and correcting for predation effects, we demonstrate that females lay a large proportion of their total complement of eggs (multiyear mean: 82.9%). The egg supplies of 17.1% of females were completely exhausted, with the remaining 82.9% of females being time limited. As predicted by theory, we estimate that even though egg limitation is a minority condition within the population, egg costs make a substantial contribution (57% of the total) to the cost of oviposition. We conclude that insect life histories evolve to produce a balanced risk of time and egg limitation and, therefore, that both of these constraining factors have important influences on insect oviposition behavior and population dynamics.     

The costs of egg production and incubation in great tits (Parus major).

The costs of egg production and incubation may have a crucial effect on avian reproductive decisions, such as clutch size and the timing of reproduction. We carried out a brood-size enlargement experiment on the great tit (Parus major), in which the birds had to lay and incubate extra eggs (full costs), only incubate extra eggs (free eggs) or did not pay any extra cost (free chicks) in obtaining a larger brood. We used female fitness (half the recruits produced plus female survival) as a fitness measure because it is the female which pays the costs of egg production and incubation, and because clutch size is under female control. Female fitness decreased with increasing costs (fitness of free chicks females is higher than that of free eggs females which is higher than that of full costs females). These fitness differences were due to differences in female survival rather than in the number of recruits produced. This is the first time that the costs of egg production and incubation have been estimated using such a complete fitness measure, including, as our measure does, the local survival to the following year of both the female and her offspring. Our results emphasize that reproductive decisions cannot be understood without taking egg production and incubation costs into account.     

Interspecific and intraspecific variations in egg hatching for British populations of Taeniopteryx nebulosa and Brachyptera risi (Plecoptera: Taeniopterygidae)

Adults were obtained from three populations of Taeniopteryx nebulosa and four populations of Brachyptera risi ; their eggs were incubated at seven constant temperatures (range 3.8–22.1°C). There were interspecific, but not intraspecific, differences in adult life-span, mean number of eggs laid per female, hatching success and egg incubation periods. The optimum temperature for hatching success and the range over which at least 50% of the eggs hatched were lower for T. nebulosa (6.5°C, 2.7–15.0°C) than for B. risi (9.0°C, 5.1–15.8°C). No eggs hatched at 22.1°C. The relationship between incubation period (d days) and water temperature (T°C) was given by; d = 326.4 T^−1.015 for T. nebulosa , d = 824.0 T^−0.739 for B. risi . Both equations successfully predicted incubation periods for eggs placed in a stream.
Hatching success and incubation periods were similar to those already published for a Norwegian population of T. nebulosa . The lack of significant intraspecific variation suggests that the genotypes associated with the variables examined in this study have remained remarkably stable in these two species in spite of the geographical isolation of their different populations.     

Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments

Abstract In many organisms, large offspring have improved fitness over small offspring, and thus their size is under strong selection. However, due to a trade-off between offspring size and number, females producing larger offspring necessarily must produce fewer unless the total amount of reproductive effort is unlimited. Because differential gene expression among environments may affect genetic covariances among traits, it is important to consider environmental effects on the genetic relationships among traits. We compared the genetic relationships among egg size, lifetime fecundity, and female adult body mass (a trait linked to reproductive effort) in the seed beetle, Stator limbatus , between two environments (host-plant species Acacia greggii and Cercidium floridum ). Genetic correlations among these traits were estimated through half-sib analysis, followed with artificial selection on egg size to observe the correlated responses of lifetime fecundity and female body mass. We found that the magnitude of the genetic trade-off between egg size and lifetime fecundity differed between environments–a strong trade-off was estimated when females laid eggs on C. floridum seeds, yet this trade-off was weak when females laid eggs on A. greggii seeds. Also differing between environments was the genetic correlation between egg size and female body mass–these traits were positively genetically correlated for egg size on A. greggii seeds, yet uncorrelated on C. floridum seeds. On A. greggii seeds, the evolution of egg size and traits linked to reproductive effort (such as female body mass) are not independent from each other as commonly assumed in life-history theory.     

The evolution of egg clustering in butterflies: A test of the egg desiccation hypothesis

Females of many insect species cluster their eggs. Egg clustering by lepidopteran species usually results in aggregation of larvae that are more often conspicuously coloured and apparently distasteful or unpalatable than larvae of solitary species. While the costs and benefits of aggregation in terms of larval survival and growth are well documented, the evolutionary ecology of egg clustering has been long debated and is still unresolved. We tested the egg desiccation hypothesis, first proposed by Stamp (1980), which to our knowledge has never been examined experimentally. The egg desiccation hypothesis proposes that egg clustering is adaptive per se (i.e. increases fitness of females) by reducing egg mortality via desiccation.We tested this hypothesis for the Nymphalid butterfly, Chlosyne lacinia, an egg-clustering species on its sunflower host plant, Helianthus annuus. We first documented natural variation in batch size for this butterfly. We then tested experimentally hatch success of varying batch sizes and egg-layering arrangements under controlled humidity levels. Hatch success was positively related to relative humidity. Eggs in larger groups with greater number of layers had greater hatch success than smaller, monolayered egg batches, especially when relative humidity was low. Our results indicate that, not only number of eggs, but also the arrangement (i.e. layering and density), increase batch survival by protecting eggs from desiccation. However, despite increased hatch success in dense, multilayered clusters, we found wide variation in layering and density in natural populations of C. lacinia. This variation is probably maintained by trade-offs in egg survival, such as increased cannibalism of eggs by siblings, in dense clusters. Nevertheless, protection from egg desiccation provides an alternative explanation for the origin and maintenance of egg clustering in lepidopterans and possibly other insects. The pattern of egg deposition in the Nymphalidae supports this hypothesis, since most North American species cluster their eggs tightly, whereas most species in tropical regions lay eggs singly or in loose monolayers.     

Energy expenditure during egg laying is equal for early and late breeding free-living female great tits

In many bird populations, variation in the timing of reproduction exists but it is not obvious how this variation is maintained as timing has substantial fitness consequences. Daily energy expenditure (DEE) during the egg laying period increases with decreasing temperatures and thus perhaps only females that can produce eggs at low energetic cost will lay early in the season, at low temperatures. We tested whether late laying females have a higher daily energy expenditure during egg laying than early laying females in 43 great tits (Parus major), by comparing on the same day the DEE of early females late in their laying sequence with DEE of late females early in their egg laying sequence. We also validated the assumption that there are no within female differences in DEE within the egg laying sequence. We found a negative effect of temperature and a positive effect of female body mass on DEE but no evidence for differences in DEE between early and late laying females. However, costs incurred during egg laying may have carry-over effects later in the breeding cycle and if such carry-over effects differ for early and late laying females this could contribute to the maintenance of phenotypic variation in laying dates.     

Larval host plant affects fitness consequences of egg size variation in the seed beetle Stator limbatus

Egg size variation often has large effects on the fitness of progeny in insects. However, many studies have been unable to detect an advantage of developing from large eggs, suggesting that egg size variation has implications for offspring performance only under adverse conditions, such as during larval competition, periods of starvation, desiccation, or when larvae feed on low-quality resources. We test this hypothesis by examining the consequences of egg size variation for survivorship and development of a seed-feeding insect, Stator limbatus, on both a low-quality (Cercidium floridum) and a high-quality (Acacia greggii) host plant. Our results are consistent with the hypothesis. S. limbatus larval performance was affected by egg size only when developing on the poor-quality host (C. floridum); larvae from large eggs survived better on C. floridum than those from small eggs, while there was no evidence of an effect of egg size on progeny development time, body weight, or survivorship when larvae developed on A. greggii. These results indicate intense selection for large eggs within C. floridum-associated populations, but not in A. greggii-associated populations, so that egg size is predicted to vary among populations associated with different hosts. Our results also support this hypothesis; females from a C. floridum-associated population (Scottsdale) laid larger eggs than females from an A. greggii-associated population (Black Canyon City).     

The consequences of adult foraging success on the components of lifetime fitness in a semelparous,sit and wait predator

Summary We evaluated the role of adult foraging success in the lifetime fitness of female crab spidersMisumena vatia. Misumena are semelparous, sit and wait predators that hunt for insect prey on flowers, in this study primarily on inflorescences (umbels) of milkweedAsclepias syriaca. We used path analysis to integrate previously performed experimental and observational studies, thereby establishing the magnitude, correlations and causal relationships of key foraging and life history variables and their roles in lifetime fitness. A path proceeding from maternal hunting patch choice through maternal mass, clutch mass and number of dispersal-age young was the dominant element and explained a large part of the variation. Other paths that incorporated parasitism of the egg mass and predation of young leaving the nests made only small impacts on variation. No trade-offs were found, primarily because a single factor, maternal mass (a maternal effect) resulting from foraging success, provided major benefits for successive life history stages. Since differences in the numbers of eggs, egg loss and mortality at dispersal resulted almost entirely from differences in maternal mass, they are controlled by the maternal generation and, thus, are appropriately attributed to the lifetime fitnesses of the mothers, rather than to those of their offspring.     

Density-dependent effects on the reproductive fitness of the New Zealand beech scale insect (Ultracoelostoma assimile) across multiple spatial scales

Abstract.  1. Intraspecific competition can be an important factor influencing the individual fitness of organisms. This study reports density-dependent effects on the fecundity of the beech scale insect ( Ultracoelostoma assimile , Hemiptera: Margarodidae) on naturally occurring, canopy-dominant red beech ( Nothofagus fusca , Fagaceae) trees in New Zealand. For the first time an increasing intensity of intraspecific competition at increasing spatial scales within individual host trees is demonstrated.
2. Beech scale insect 'tests' containing adult female scale insects and eggs were collected from the trunks of 10 red beech trees [17.7–48.5 cm in diameter at breast height (1.4 m), d.b.h.] with varying densities of scale insect infestation. The relationship between individual female fecundity and scale insect density at three spatial scales: local (within 5 cm), lower trunk (below 2 m above ground level), and whole tree, was tested.
3. Beech scale insect fecundity was density dependent, with total female egg load decreasing with increasing scale insect density. The strength of the density-dependent effect increased with increasing spatial scale, suggesting that scale insects are creating a tree-wide drain on the quality of phloem sap, rather than depleting nutrients from localised, high-density areas within trees. These results indicate that at high densities, the New Zealand beech scale insect can have a negative effect on the nutritional quality of the phloem of red beech, thus negatively affecting conspecifics elsewhere on individual host trees. The increasing intensity of the effect with increasing spatial scale within individual trees emphasises the importance of measuring density-dependent effects at the appropriate spatial scale.