THE RELATIVE CONTRIBUTIONS OF TIME AND EGGS TO THE COST OF REPRODUCTION

Whether the trade-off between current and future reproduction in insect parasitoids is mediated by the costs of time or eggs remains an issue of contention. Life-history models predict that parasitoids have some risk of exhausting their lifetime supply of oocytes. I develop a simple conceptual model that assesses the relative contributions of time and eggs to the cost of reproduction by placing them in a common currency: foregone future fitness returns. Although rates of egg limitation observed in nature are modest, eggs still often make the dominant contribution to the overall cost of oviposition. Therefore, models of parasitoid reproduction must recognize the costliness of both time and eggs.     

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.     

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.     

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.     

Costs of mating and egg production in female Callosobruchus chinensis

Costs of reproduction include the costs of mating and egg production. Specific techniques such as irradiation or genetic mutation have been used to divide the expense into costs of mating and egg production in previous studies. We tried to divide the costs in the adzuki bean beetle, Callosobruchus chinensis (Coleoptera: Bruchidae), which needs some kinds of bean as an oviposition substrate. Mated females that were not allowed to lay eggs had a shorter life span than virgin females, but they had a longer life span than mated females that were allowed to lay eggs. The results showed two independent significant costs, mating and egg production, on the life span in C. chinensis. Costs of mating, however, include the costs of sexual harassment by males and copulation itself, and we need further studies to divide the costs. The present method for dividing the cost of reproduction into costs of mating and egg production can be applied to a broad taxonomic range of insect species, and thus it will be a useful model system for inter-specific comparisons of costs of mating and egg production.     

Developmental response to a seasonal time constraint: the effects of photoperiod on reproduction in the grasshopper Romalea microptera

Abstract.  1. Some organisms respond adaptively to seasonal time constraints by altering development time to life-history transitions (e.g. metamorphosis, oviposition). Such life-history changes may have costs (e.g. reduced fecundity, mass, offspring quality).
2. The hypothesis that a northern population of the grasshopper Romalea microptera (Beauvois) would show adaptive plasticity in oviposition timing in response to seasonal time constraints was tested by manipulating photoperiod to simulate the middle of the active season (Long photoperiod), the end of the active season (Short photoperiod), and seasonal change (photoperiod Declining from long to short). Females received either high or low food rations. Short or Declining photoperiod were predicted to induce early oviposition with costs of reduced egg number, post-oviposition mass, or egg size, particularly in low-food females.
3. Effects of food ration and photoperiod, but not interaction, were significant in failure time analysis of age at oviposition. mancova on age at oviposition, egg number, and post-oviposition mass yielded similar effects. The multivariate effect of photoperiod resulted primarily from reduced time to oviposition in Short or Declining photoperiod. No costs in egg number or post-oviposition mass were associated with this photoperiod-induced reduction in time to oviposition. The multivariate effect of food ration resulted mainly from lower egg number with low food. Food ration affected egg size, but photoperiod and interaction did not. In all cases, Short and Declining photoperiod produced similar effects.
4. In its northern range, R. microptera accelerates reproduction in response to seasonal constraints, a response that may be adaptive. How R. microptera avoids costs associated with this reduced pre-oviposition period remains unknown.     

Ovarian dynamics, egg size, and egg number in relation to temperature and mating status in a butterfly

Although the temperature‐size rule, that is, an increase in egg (and body) size at lower temperatures, applies almost universally to ectotherms, the developmental mechanisms underlying this consistent pattern of phenotypic plasticity are hitherto unknown. By investigating ovarian dynamics and reproductive output in the tropical butterfly Bicyclus anynana (Butler) (Lepidoptera: Nymphalidae: Satyrinae) in relation to oviposition temperature and mating status, we tested the relevance of several competing hypotheses for temperature‐mediated variation in egg size and number. As expected, females ovipositing at a lower temperature laid fewer but larger eggs than those ovipositing at a higher temperature. Despite pronounced differences in egg‐laying rates, oocyte numbers were equal across temperatures at any given time, while oocyte size increased at the lower temperature. In contrast, there were greatly reduced oocyte numbers in mated compared to virgin females. Our results indicated that temperature‐mediated plasticity in egg size cannot be explained by reduced costs of somatic maintenance at lower temperatures, enabling the allocation of more resources to reproduction (reproductive investment was higher at the higher temperature). Furthermore, there was no indication for delayed oviposition (no accumulation of oocytes at the lower temperature, in contrast to virgin females). Rather, low temperatures greatly reduced the oocyte production (i.e., differentiation) rate and prolonged egg‐maturation time, causing low egg‐laying rates. Our data thus suggested that oocyte growth is less sensitive to temperature than oocyte production, resulting in a lower number of larger eggs at lower temperatures.     

A fecundity cost of (walking) mobility in an insect

Evolutionary theory predicts trade‐offs between fecundity and mobility, but there is substantial lack of empirical evidence if and how basic mobility relates to fitness costs. In a field experiment, we investigated fecundity costs of mobility in a non‐migratory, wing‐monomorphic grasshopper, Stenobothrus lineatus, and at the same time tested for possible effects of reproductive state (egg‐load) on the mobility. For 10 days, body weight and activity radius of 60 females were recorded daily and oviposition events were inferred from abrupt weight losses. We found a strong and significant relationship between the individual mobility and the time between egg pods laid (interpod period). Individual egg‐laying was reduced by a rate of 0.36 eggs per day with each meter increase in mean daily activity radius. The trade‐off was not biased by the size of the females, that is, constitution did not positively influence both offspring number and mobility. Egg‐load had no significant influence on the individual distances travelled. We could demonstrate that mobility – as induced and selected for by foraging, thermoregulation, predator escape, shelter seeking, and reproduction – can be directly paid off by fecundity. This direct consequence of mobility on individual fitness was detected for the first time in a walking insect.     

The effect of egg load on readiness to accept a low-quality host plant is weak and age dependent in a geometrid moth

Abstract.  1. Most empirical and theoretical studies treat egg load as a major determinant of insect oviposition behaviour, and predict a positive link between egg load and readiness to oviposit.
2. In the present study, the correlation between egg load and readiness to lay eggs on a low-ranked host was examined in wild-caught moths, Scotopteryx chenopodiata L. (Lepidoptera: Geometridae).
3. No overall effect of egg load on oviposition could be detected. However, there was a significant interaction between egg load and wing wear: in only one wing-wear class, out of four, high egg load tended to promote oviposition, while in the three other classes the effect was insignificant.
4. The results suggest that the effect of egg load on oviposition may depend on the age of the ovipositing insect.     

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.     

Plasticity and canalization in the control of reproduction in the lubber grasshopper

The ability to change reproductive tactics during adult developmentin response to environmental variation is predicted to enhancefitness. Many organisms show phenotypic plasticity early innon-embryonic development, but later exhibit phases of developmentalinflexibility (=canalization). Therefore, we studied reproduction-relatedhormones and proteins and their relationships to plasticityin the Eastern lubber grasshopper. Diet-switching experimentsdemonstrated plasticity early in the egg production cycle, buta switch to canalization late in the cycle. We measured developmentaltiters of 4 hemolymph compounds from single individuals fromadult molt until first oviposition. These 4 compounds were theegg-yolk precursor protein vitellogenin, juvenile hormone (thecentral regulator of insect reproduction), major hemolymph proteins,and ecdysteroids (the arthropod molting hormone that ultimatelyis stored in the egg). Using diet manipulations, we investigatedhow these developmental titers relate to the switch from plasticto canalized egg production. All 4 hemolymph compounds reachedtheir peak levels during the canalized phase, about 12 day beforeoviposition. Diet switches after these peak levels did not affectthe timing to oviposition. Therefore, these peak titers werephysiological events that occurred after the individual committedto laying. We compared these patterns in reproduction to thedevelopment toward adult molt, another major life-history eventin insects. We observed an extended canalized phase before theadult molt. This canalized phase always included a peak of ecdysteroids.The similar patterns in the physiology of these life-historyevents suggested that common limitations may exist in majordevelopmental processes of insects that are directed by hormones.     

Size‐induced phenotypic reaction norms in a parasitoid wasp: an examination of life‐history and behavioural traits

The amount of resources available during development often affects body size, causing phenotypic variation in life‐history traits and reproductive behaviours. However, past studies have seldom examined the reaction norms of both life‐history and behavioural traits versus body size. We measured the phenotypic plasticity of several life‐history (age‐specific egg load, egg size, longevity) and behavioural (oviposition rate, host marking rate, walking speed) traits of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) in response to body size variation. We predicted that life‐history traits would show more evidence of size compensation than behavioural traits, resulting in fewer positively‐sloped size versus trait reaction norms among the former. As predicted by life‐history models, smaller wasps appear to shift resource allocation towards early‐life reproduction, having a similar egg load to large individuals 9 days after emergence. Surprisingly, longevity was unaffected by body size. However, egg size, the number of offspring produced during oviposition bouts, and the rate of subsequent egg synthesis were greater for larger individuals. In addition, as predicted, the reaction norms of behavioural traits versus body size were all positively sloped. Thus, despite possible adaptive compensatory plasticity of life‐history traits by small individuals, behavioural constraints directly related to body size would contribute to maintaining a positive size–fitness relationship.     

Responses of ovipositing moths to host plant deprivation: life history aspects and implications for intercropping

1. When considering intercropping as a strategy to reduce pest oviposition, knowledge about the insect’s oviposition behaviour is very important. Physiological effects on the insect because of difficulties in finding a suitable oviposition site may also be important. 2. In the present study, the effects that delays in access to host plants have on lifetime fecundity on diamondback moth and leek moth were examined. The ability to postpone egg laying, fecundity and lifetime oviposition are discussed in relation to intercrop/cover crop as a strategy to reduce oviposition on crop plants. 3. When faced with host plant deprivation, the diamondback moth is relatively more dependent upon host plant stimuli for the onset of egg production. By contrast, leek moth is able to postpone egg production for a longer time. There even appeared to be a tendency for leek moth females to extend their lifetime when faced with host plant deprivation. 4. We conclude that leek moths have the ability to postpone production of eggs and lay them later in life when finally encountering host plants after a period of host plant deprivation. Therefore, the use of intercropping as a strategy to reduce oviposition is questionable. For such an insect, use of a trap crop might be a better option because the female will lay her eggs in the trap crop and not get the opportunity to lay them later in life when finally encountering crop plants.     

Experimental evidence of early costs of reproduction in conspecific viviparous and oviparous lizards

Reproduction entails costs, and disentangling the relative importance of each stage of the reproductive cycle may be important to assess the costs and benefits of different reproductive strategies. We studied the early costs of reproduction in oviparous and viviparous lizard females of the bimodal reproductive species Zootoca vivipara. Egg retention time in oviparous females is approximately one-third of the time in viviparous females. We compared the vitellogenesis and egg retention stages that are common to both reproductive modes. Precisely, we monitored the thermoregulatory behaviour, the weight gain and the immunocompetence of the females. Moreover, we injected an antigen in half of the females (immune challenge) to study the trade-offs between reproductive mode and immune performance and between different components of the immune system. Finally, we experimentally induced parturition in viviparous females at the time of egg laying in oviparous females. Oviparous and viviparous females did not show strong differences in response to the immune challenge. However, viviparous females spent more time thermoregulating while partially hidden and gained more weight than oviparous females. The greater weight gain indicates that the initial period of egg retention is less costly for viviparous than for oviparous females or that viviparous females are able to save and accumulate energy at this period. This energy may be used by viviparous females to cope with the subsequent costs of the last two-third of the gestation. Such an ability to compensate the higher costs of a longer egg retention period may account for the frequent evolution of viviparity in squamate reptiles.     

Experience‐ and age‐mediated oviposition behaviour in the yellow fever mosquito Stegomyia aegypti (=Aedes aegypti)

In repeated behaviours such as those of feeding and reproduction, past experiences can inform future behaviour. By altering their behaviour in response to environmental stimuli, insects in highly variable landscapes can tailor their behaviour to their particular environment. In particular, female mosquitoes may benefit from plasticity in their choice of egg‐laying site as these sites are often temporally variable and clustered. The opportunity to adapt egg‐laying behaviour to past experience also exists for mosquito populations as females typically lay eggs multiple times throughout their lives. Whether experience and age affect egg‐laying (or oviposition) behaviour in the mosquito Stegomyia aegypti (=Aedes aegypti) (Diptera: Culicidae) was assessed using a wind tunnel. Initially, gravid mosquitoes were provided with a cup containing either repellent or well water. After ovipositing in these cups, the mosquitoes were blood‐fed and introduced into a wind tunnel. In this wind tunnel, an oviposition cup containing repellent was placed in the immediate vicinity of the gravid mosquitoes. A cup containing well water was placed at the opposite end of the tunnel so that if the females flew across the chamber, they encountered the well water cup, in which they readily laid eggs. Mosquitoes previously exposed to repellent cups became significantly more likely to later lay eggs in repellent cups, suggesting that previous experience with suboptimal oviposition sites informs mosquitoes of the characteristics of nearby oviposition sites. These results provide further evidence that mosquitoes modify behaviour in response to environmental information and are demonstrated in a vector species in which behavioural plasticity may be ecologically and epidemiologically meaningful.     

Using sex ratios to estimate what limits reproduction in parasitoids

The reproductive success of a foraging parasitoid may be limited by the number of eggs that she produces and/or the number of hosts that she can locate. Despite the significance for population dynamics and numerous areas of behavioural ecology, the relative importance of these factors remains an issue of contention. Attempts to resolve this controversy have been hindered because estimating the importance of factors limiting reproduction in the field can be extremely laborious and time consuming. We show how sex ratio data can be used as a relatively easy method to indirectly estimate the relative importance of the factors limiting reproduction. Sex ratio data from 48 samples of eight species suggest that: (a) the extent of host or egg limitation in a species varies between site collected and time of year; and (b) on average, species are at an intermediate position on the egg/host limitation continuum, with a bias towards host limitation.     

Fitness and feeding are affected in the two-spotted stinkbug,Perillus bioculatus,by the cysteine proteinase inhibitor,oryzacystatin I

Plant resistance to insect pests based on recombinant proteinase inhibitors (Pis) could interfere with natural enemies of target pests, as their own proteolytic systems may also be sensitive to large spectrum PIs. Oryzacystatin I (OCI) is a potential insect pest resistance factor currently engineered into a variety of crop plants, including potato Solanum tuberosum. Potential for OCI interfering with female reproduction in Perillus bioculatus, a stinkbug predator of Colorado potato beetle, Leptinotarsa decemlineata, was studied by chronic feeding for 18 days on prey loaded with 1–16 μg OCI/day. Mortality of treated females was negligible, but fertility was reduced by up to 50%. Additional dose-dependent effects in reproducing females included delayed oviposition, reduced fecundity, lower egg mass size, and reduced egg eclosion incidence. Females fed for 18 days on OCI at ≤4 μg/day returned to normal oviposition when switched to prey without OCI after 18 days of treatment, but negative effects persisted for at least 10 days at higher doses. Affected reproduction in P. bioculatus is consistent with the use of OCI-sensitive digestive proteinases by this stinkbug. However, azocaseinase activity in whole body extracts of OCI-fed females increased about twofold indicating compensation, and OCI-sensitive proteinases were still present in extracts. When timed for delay to trigger attack on Colorado potato beetle larvae under controlled conditions, stinkbugs feeding on OCI appeared consistently hungrier than controls fed at similar rate, suggesting that predation by stinkbugs exposed to OCI-recombinant foliage would be higher than normal. Arch. Insect Biochem. Physiol. 38:74–83, 1998. © 1998 Wiley-Liss, Inc.     

Reproductive allocation and the long-term costs of reproduction in Siparuna grandiflora, a dioecious neo-tropical shrub

1 Using a combination of observational and experimental approaches, both allocation of resources to reproduction (often called the direct cost of reproduction) and the subsequent long-term costs (the indirect, delayed or demographic cost) associated with reproductive allocation to male and female function in Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub, were examined.
2 The objectives were to determine whether females allocate more biomass or nitrogen per reproductive episode than males, and whether there is a long-term cost of reproduction in terms of subsequent growth or reproduction for either sex. If there is no long-term cost of reproduction, then reproduction may be viewed as free in an evolutionary sense.
3 As is generally the case in dioecious species, females allocated more biomass and nitrogen to reproduction than males. Females also showed delayed costs of reproduction in terms of decreased growth and subsequent reproduction, whereas males did not.
4 The lack of measurable delayed costs in males suggests that with the evolution of dioecy, selection has reduced delayed costs of reproduction in S. grandiflora males. In contrast, females that were prevented from reproducing were able to re-allocate resources to growth, and produced more stem length on average than males. This re-allocation response may have evolved to reduce delayed costs of reproduction in females over time frames longer than that considered in the present study.     

Mating in aphidophagous ladybirds: costs and benefits

Abstract:  Mating costs and benefits were studied in three aphidophagous ladybirds, viz. Cheilomenes sexmaculata , Coccinella septempunctata and Propylea dissecta by subjecting them to different numbers of matings. Longevity, fecundity and percent egg viability were regressed with number of matings to determine the costs and trade-offs, if any. Longevity decreased with increasing number of matings in both C. sexmaculata and P. dissecta indicating a cost of mating. The lack of such a cost in C. septempunctata has been ascribed to spermatophore consumption by females of this ladybird. Both fecundity and percent egg viability increased with increasing number of matings and are probably indicative of the benefits. Short-lived females distributed their reproduction uniformly in their lifetime while long-lived females showed a high burst of reproductive activity followed by a gradual decline. Percent egg viability decreased after the completion of the requisite number of matings.