Lack of lipogenesis in parasitoids: a review of physiological mechanisms and evolutionary implications

The ability of organisms to adapt to fluctuating food conditions is essential for their survival and reproduction. Accumulating energy reserves, such as lipids, in anticipation of harsh conditions, will reduce negative effects of a low food supply. For Hymenoptera and Diptera, several parasitoid species lack adult lipogenesis, and are unable to store excess energy in the form of lipid reserves. The aim of this review is to provide a synthesis of current knowledge regarding the inability to accumulate lipids in parasitoids, leading to new insights and prospects for further research. We will emphasize physiological mechanisms underlying lack of lipogenesis, the evolution of this adaptation in parasitoids and its biological implications with regard to life history traits. We suggest the occurrence of lack of lipogenesis in parasitoids to be dependent on the extent of host exploitation through metabolic manipulation. Currently available data shows lack of lipogenesis to have evolved independently at least twice, in parasitic Hymenoptera and Diptera. The underlying genetic mechanism, however, remains to be solved. Furthermore, due to the inability to replenish adult fat reserves, parasitoids are severely constrained in resource allocation strategies, in particular the trade-off between survival and reproduction.     

Lifetime allocation of juvenile and adult nutritional resources to egg production in a holometabolous insect.

In holometabolous insects reproductive success is strongly determined by the nutritional resources available to the females. In addition to nutrients derived from adult feeding, resources for egg production may come from the limited reserves accumulated during the larval stages. The pattern of allocation of these larval reserves to egg production is expected to be strongly linked to the nutritional ecology of the adult. We investigate the temporal pattern of allocation of larval reserves to reproduction in a host-feeding parasitoid wasp. As predicted by the dynamics of allocation of an adult meal, larval reserves are the main source of nutrients for four or five days after emergence. However, despite the high frequency of host feeding and the high nutrient content of a haemolymph meal, which we predicted would lead to larval reserves being conserved in the event of host deprivation, larval reserves contribute to egg production throughout the lifetime of the female. We propose several mechanistic and adaptive explanations for our results, including the possible existence of a limiting or key nutrient for egg production of exclusively larval origin. We make further predictions concerning the pattern of allocation of larval resources in parasitoids with different adult nutritional requirements.     

Geographic Variation of Photoperiodic Diapause but Not Adult Survival or Reproduction of the Invasive Mosquito Aedes albopictus (Diptera: Culicidae) in North America

Climate differences across latitude can result in seasonal constraints and selection on life-history characters. Because Aedes albopictus (Skuse) invaded North America in the mid-1980s, it has spread across a range of ≈14° latitude and populations in the north experience complete adult mortality because of cold winter temperatures that are absent in the south. Life-table experiments were conducted to test for differences in the adult survival and reproductive schedules of Ae. albopictus females from three populations from the northern (Salem, NJ; Springfield, IL; Eureka, MO; ≈39° N) and southern (Palm Beach, Palmetto, Tampa, FL; ≈27-28° N) extremes of the species distribution in North America. There were consistent differences between northern and southern populations in incidence of photoperiodically-induced egg diapause. Under short daylength, diapause eggs constituted twice the proportion of total viable eggs from northern females (81.9-92.1%) than southern females (35.9-42.7%). There were no consistent differences between northern and southern populations in resource allocation between reproduction and maintenance, reproduction over time, and reproductive investment among offspring, and no apparent trade-offs between diapause incidence with reproduction or longevity. Our results suggest that the main response of North American Ae. albopictus to unfavorable winter climates is via the life history strategy of producing diapausing eggs, rather than quantitative variation in reproduction, and that there are no detectable costs to adult survival. Inherent geographic variation in the expression of diapause, consistent with the latitudinal extremes of A. albopictus, indicates evolutionary loss of diapause response in southern populations because of the invasion of A. albopictus in North America.     

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.     

Geographic variation in host-selection behaviour in the Drosophila parasitoid Leptopilina clavipes

In parasitoid wasps, the process of locating and selecting suitable oviposition sites is under strong selection due to the direct linkage of successful host selection and female fitness. Leptopilina clavipes Hartig (Hymenoptera: Figitidae) is a parasitoid wasp of larvae of several Drosophila species that occurs over Western Europe, where it shows genetic differentiation between populations from northern and southern Europe. It is expected to experience differential selection pressures on both physiological (survival) and behavioural (host selection) components of foraging, because it occurs over a broad geographic range. We investigated whether the genetic differentiation in L. clavipes is linked to differentiation in both the physiological and behavioural components of foraging. We compared survival and host‐selection behaviour of two L. clavipes strains, one originating from northwestern Europe and one from southern Europe. In a series of choice experiments, females were offered pairs of larvae from three host species that are present in both regions, but use different breeding substrates: Drosophila phalerata Meigen (fungi), Drosophila subobscura Collin (rotting plant material, fungi, and fermenting fruits), and Drosophila melanogaster Meigen (fermenting fruits) (all Diptera: Drosophilidae). Survival patterns across the three host species were similar for both L. clavipes strains. Host‐selection behaviour did differ, where parasitoids from southern Europe accepted all hosts offered, while parasitoids from northwestern Europe were more specialists and accepted hosts breeding in fungi, but were reluctant towards D. melanogaster. This differentiation in host‐selection behaviour reflects the genetic differentiation present in European L. clavipes and shows adaptation to local differences in host communities.     

Comparing resource exploitation and allocation of two closely related aphid parasitoids sharing the same host

Species belonging to the same guild (i.e. sharing the same resources) can reduce the negative effects of resource competition through niche partitioning. Coexisting species may differ in their resource exploitation and in the associated allocation of nutrients, depending on their resource niche. Trade-offs in nutrient allocation, such as between reproduction and survival, or between early and late reproduction, are moderated by the abundance and distribution of resources. In this study we investigate differences in larval resource exploitation and adult reproductive strategy of two sympatric aphid parasitoids sharing a common host. The habitat specialist Aphidius rhopalosiphi and the generalist Aphidius avenae occur in cereal crops of Western Europe, where both species attack the major host resource: the grain aphid Sitobion avenae. For this purpose, we measured their acquisition of capital lipid resources, their age-specific fecundity and reproductive effort, their life span and their metabolic rate. We found that these species do not differ neither in larval lipid accumulation nor in the number of eggs at emergence and the timing of egg production, but diverge in other adult reproductive strategies. The rate of adult egg production was higher in A. rhopalosiphi than A. avenae, but at the expense of producing smaller eggs. Throughout adult life, reproductive effort was higher in A. avenae, perhaps facilitated by its higher metabolic rate than A. rhopalosiphi. The divergence between species in life history syndromes likely reflects their adaptations to their resource niche. A high egg production probably allows the specialist A. rhopalosiphi to exploit more S. avenae individuals in cereal crops, while the generalist A. avenae because of its variety of hosts, maximizes the investment per egg but at the expense of a lower lifespan. Our results suggest that differential resource allocation may be a more common pattern that promotes coexistence of species within a guild.     

Optimal resource allocation to survival and reproduction in parasitic wasps foraging in fragmented habitats

Expansion and intensification of human land use represents the major cause of habitat fragmentation. Such fragmentation can have dramatic consequences on species richness and trophic interactions within food webs. Although the associated ecological consequences have been studied by several authors, the evolutionary effects on interacting species have received little research attention. Using a genetic algorithm, we quantified how habitat fragmentation and environmental variability affect the optimal reproductive strategies of parasitic wasps foraging for hosts. As observed in real animal species, the model is based on the existence of a negative trade-off between survival and reproduction resulting from competitive allocation of resources to either somatic maintenance or egg production. We also asked to what degree plasticity along this trade-off would be optimal, when plasticity is costly. We found that habitat fragmentation can indeed have strong effects on the reproductive strategies adopted by parasitoids. With increasing habitat fragmentation animals should invest in greater longevity with lower fecundity; yet, especially in unpredictable environments, some level of phenotypic plasticity should be selected for. Other consequences in terms of learning ability of foraging animals were also observed. The evolutionary consequences of these results are discussed.     

Geographic variation in reproductive success of the parasitoid Asobara tabida in larvae of several Drosophila species

Abstract.

• 1 Asobara tabida is a parasitoid of Drosophila larvae in fermenting substrates. Because it is a widespread species, it may encounter different biotic and abiotic circumstances in various parts of its range.
• 2 The species composition of the host population varies over the parasitoid's range: D.obscura-group species (especially D.subobscura) are the main hosts for northwestern and central European parasitoids; D.melanogaster is the main host for southern European parasitoids.
• 3 D.melanogaster larvae can defend themselves against A.tabida by encapsulating the parasitoid egg, and survival in D.melanogaster is always lower than in D.subobscura.
• 4 Parasitoids from southern European populations are much better able to survive in D.melanogaster than their northwestern and central European conspecifics; parasitoids from different populations are equally well able to survive in D.subobscura.
• 5 The lower survival in D.melanogaster may be partly compensated for by the larger size of parasitoids emerging from this host species compared to parasitoids emerging from D.subobscura.
• 6 Within population groups, larger A.tabida females have more eggs in their ovarioles. Additionally, southern European females have more eggs and less fat than northern and western/central European females. The relationship between size and longevity is ambiguous.
• 7 It is concluded that parasitoids from different populations are adapted to region-specific circumstances.

     

Impact of tree leaf phenology on growth rates and reproduction in the spring flowering species Trillium erectum (Liliaceae)

We investigated the impact of overstory tree leaf phenology on growth rates, carbon allocation pattern, and fruit characteristics in the spring flowering species, Trillium erectum (Liliaceae). Air temperature, overstory canopy closure, and T. erectum phenology were monitored at three locations following a latitudinal gradient in Québec, Canada. Northern sugar maple trees leaf out at cooler temperatures than more southern populations, while Trillium development was initiated at the same soil temperature irrespective of the latitude. Therefore, in northern areas, the time between initiation of T. erectum leaf expansion and canopy closure was shorter than in southern areas, which left less time for northern plants to accumulate reserves before canopy closure. Differences in growth patterns were noted between T. erectum populations. From a south-north gradient, investment to reproduction, total plant biomass, and annual growth rate decreased, while specific leaf area and stem height increased, indicating shade acclimation. The length of the high light period in early spring seems to be a determinant for spring flowering plants' growth and reproduction and may explain the northern distribution limit of some of these species.     

Income resources and reproductive opportunities change life history traits and the egg/time limitation trade‐off in a synovigenic parasitoid

1. Synovigenic parasitoids emerging with no or only a few mature oocytes could not rely on only capital resources, but also need to acquire income resources. Income resources in nature can either contribute to egg maturation as a food resource and/or create unpredictability in realised reproductive opportunities for synovigenic parasitoids. Therefore, we hypothesised such resources could affect life history traits and the risks of egg/time limitation in synovigenic parasitoids. 2. Using the Ovigeny Index, we investigated the effects of various host availability levels (unavailable, limited, and unlimited availability) and non‐host foods (water and honey) on life history traits and on the occurrence of egg/time limitation in Eretmocerus hayati, a predominant parasitoid on Bemisia tabaci. 3. The Ovigeny Index of Er. hayati was 0.28, which suggested it was a typical synovigenic species. Both host availability levels and non‐food type had major effects on life history traits of this parasitoid, but the availability of hosts for both feeding and reproduction was the key factor. Meanwhile, egg/time limitation was encountered by all wasps and its intensity varied with host availability levels. 4. Our results confirmed that the income resource and reproductive opportunity played a central role in shaping the life history and risks of egg/time limitation of a synovigenic parasitoid.     

Vector competence of northern and southern European Culex pipiens pipiens mosquitoes for West Nile virus across a gradient of temperatures

In Europe, West Nile virus (WNV) outbreaks have been limited to southern and central European countries. However, competent mosquito vectors and susceptible bird hosts are present in northern Europe. Differences in temperature and vector competence of mosquito populations may explain the absence of WNV outbreaks in northern Europe. The aim of the present study was to directly compare vector competence of northern and southern European Culex pipiens (Cx. p.) pipiens mosquitoes for WNV across a gradient of temperatures. WNV infection and transmission rates were determined for two Cx. p. pipiens populations originating from The Netherlands and Italy, respectively. Mosquitoes were orally exposed by providing an infectious bloodmeal, or by injecting WNV (lineage 2) in the thorax, followed by 14‐day incubation at 18, 23, or 28 °C. No differences in infection or transmission rates were found between the Cx. p. pipiens populations with both infection methods, but WNV transmission rates were significantly higher at temperatures above 18 °C. The absence of WNV outbreaks in northern Europe cannot be explained by differences in vector competence between Cx. p. pipiens populations originating from northern and southern Europe. This study suggests that low temperature is a key limiting factor for WNV transmission.     

The combined effect of host and food availability on optimized parasitoid life‐history traits based on a three‐dimensional trade‐off surface

The reproductive success of many insects is considered to be limited by two main factors: the availability of mature eggs to lay (termed egg limitation) and the time to locate suitable hosts (termed time limitation). High host density in the environment is likely to enhance oviposition opportunities, thereby selecting for higher investment in egg supply. In contrast, a shortage of food (e.g. sugar sources) is likely to increase the risk of time limitation, thereby selecting for higher allocation to initial energy reserves. To our knowledge, the combined effect of host and food availability on these optimal life‐history allocations has never been investigated. We thus modelled their simultaneous effects on a three‐dimensional trade‐off between initial investment in energy reserves, egg number and egg size, while focusing on insect parasitoids. The model was based on Monte Carlo simulations coupled with genetic algorithms, in order to identify the optimal life‐history traits of a single simulated parasitoid female in an environment in which both hosts and food are present in varying densities. Our results reproduced the simple predictions described above. However, some novel predictions were also obtained, especially when specific interactions between the different factors were examined and their effects on the three‐dimensional life‐history surface were considered. The work sheds light on long‐lasting debates regarding the relative importance of time versus egg limitation in determining insect life‐history traits and highlights the complexity of life‐history evolution, where several environmental factors act simultaneously on multiple traits.     

Evolutionary constraints on polyembryony in parasitic wasps: a simulation model

Polyembryony involves the production of several genetically identical progeny from a single egg through clonal division. Although polyembryonic development allows highly efficient reproduction, especially in some parasitoid wasps, it is far less common than monoembryony (development of one embryo per egg). To understand what might constrain the evolutionary success of polyembryony in parasitoids, we developed Monte Carlo models that simulate the competition between polyembryonic females and their monoembryonic counterparts. We investigated which simulated life‐history traits of the females allow the monoembryonic mode of development to succeed. Published empirical studies were surveyed to explore whether these traits indeed differ between polyembryonic parasitoids and related monoembryonic species. The simulations predict an advantage to monoembryony in parasitoids whose reproduction is limited by host availability rather than by egg supply, and that parasitize small‐bodied hosts. Comparative data on the parasitoid families Encyrtidae and (to a lesser extent) Braconidae, but not the data from Platygastridae, circumstantially support these predictions. The model also predicts monoembryony to outcompete polyembryony when: 1) hosts vary considerably in quality, 2) polyembryonic development carries high physiological costs, and 3) monoembryonic females make optimal clutch size decisions upon attacking hosts. These multiple constraints may account for the rarity of polyembryony among parasitoid species.     

Manipulation of parasitoid size using the temperature-size rule: fitness consequences

The phenotypic effects of rearing temperature on several fitness components of the koinobiont parasitoid, Aphidius colemani, were examined. Temperatures experienced during development induced a plastic linear response in the dry and fat masses of the immature stage and a non-linear response in the growth rate as well as in the size of adults. We investigated if the phenotypic morphometrical plasticity exhibited by parasitoids reared at different temperatures can induce variations in fitness-related traits in females. We did not find any difference in immature (pupal) mortality in accordance to rearing temperature. However, when examining adult longevity, we found an inverse linear relation with developmental temperature, confirming the usual rule that larger and fatter wasps live longer than smaller ones. The pattern of female fecundity was non-linear; wasps that developed at high and low temperatures were less productive. We suggest that when development is short, the accumulated reserves are not adequate to support both fecundity and survival. By manipulating adult size through changes in the rearing temperature, we showed that the usual shape of the size/fitness function is not always linear as expected. Developmental temperature induced a plasticity in energy reserves which affected the functional constraints between survival and reproduction.     

Intraspecific variability in egg maturation patterns and associated life‐history trade‐offs in a polyembryonic parasitoid wasp

1. Life‐history theory predicts a trade‐off between the resources allocated to reproduction and those allocated to survival. Early maturation of eggs (pro‐ovigeny) is correlated with small body size and low adult longevity in interspecific comparisons among parasitoids, demonstrating this trade‐off. The handful of studies that have tested for similar correlations within species produced conflicting results. 2. Egg maturation patterns and related life‐history traits were studied in the polyembryonic parasitoid wasp, Copidosoma koehleri (Hymenoptera: Encyrtidae). Although the genus Copidosoma was previously reported to be fully pro‐ovigenic, mean egg loads of host‐deprived females almost doubled within their first 6 days of adulthood. 3. The initial egg‐loads of newly emerged females were determined and age‐specific realised fecundity curves were constructed for their clone‐mate twins. The females' initial egg loads increased with body size, but neither body size nor initial egg load was correlated with longevity and fecundity. 4. The variation in initial egg loads was lowest among clone‐mates, intermediate among non‐clone sisters and highest among non‐sister females. The within‐clone variability indicates environmental influences on egg maturation, while the between‐clone variation may be genetically based. 5. Ovaries of host‐deprived females contained fewer eggs at death (at ～29 days) than on day 6. Their egg loads at death were negatively correlated with life span, consistent with reduced egg production and/or egg resorption. Host deprivation prolonged the wasps' life span, suggesting a survival cost to egg maturation and oviposition. 6. It is concluded that adult fecundity and longevity were not traded off with pre‐adult egg maturation.     

Life history correlations: why are hymenopteran parasitoids an exception?

This study compares the life histories of five hymenopteran species (genus Leptopilina ), and aims to identify reasons why developmental time and life span are not correlated in parasitic Hymenoptera, a relationship that is present in many other taxa. Developmental time, life span, body size, and related traits were measured in female parasitoids that eclosed either from hosts of a standard species or from the host species that are naturally used. Phylogenetic controlled tests revealed that body size was positively correlated with fat reserves, starvation time, and egg load. Developmental time was neither correlated with life span nor correlated to host developmental time. We suggest two mechanisms that affect a potential relationship between developmental time and life span in Leptopilina : (i) delayed emergence in species that live in a stochastic environment (fungi), and (ii) host species related plasticity for growth rates. Additionally, variable adult feeding conditions have large effects on life span measures.     

Lizards combine stored energy and recently acquired nutrients flexibly to fuel reproduction

1. Energy allocation strategies for reproduction are viewed typically as a continuum between reliance on 'income' (recently acquired energy) vs. 'capital' (stored reserves) for fuelling reproduction. Because ectothermy facilitates long-term energy storage and often involves low feeding rates, traditional views suggest that many ectotherms rely heavily on stored reserves for egg production. 2. We explored the temporal relationship between energy intake and expenditure in a multi-clutching lizard (Amphibolurus muricatus) by evaluating the effect of maternal nutrition on reproductive output and by contrasting delta(13)C measurements of the maternal diet and endogenous energy stores with that of the eggs produced. 3. Our experiment revealed that females utilize both endogenous energy stores and recently acquired food to fuel reproduction; this pattern did not shift seasonally from first to second clutches produced. Importantly, however, egg lipid was derived primarily from capital, whereas egg protein was derived about equally from both income and capital. 4. Overall, these results suggest that the energy allocation strategy used for reproduction differs among egg components, and that the use of recently acquired energy for reproduction may be more widespread in ectotherms than thought previously.     

Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia)

This study focuses on the seasonal accumulation and depletion of somatic energy in the Atlantic silverside (Menidia menidia), an annual estuarine fish. Previous research revealed that northern silversides are subject to strong size-dependent winter mortality, while southern fish suffer no appreciable winter mortality. To examine whether there was geographic differentiation in allocation strategies, we compared temporal patterns of energy storage and utilization among three populations along this gradient in seasonality. The comparative design used monthly or biweekly samples of fish collected in the wild, as well as samples of fish from each population reared in a common environment, where genetic differences can be clarified. Somatic energy stores were quantified via gravimetric analysis of neutral storage lipids and lean tissue. Analysis revealed that small individuals maintained relatively low levels of lipid reserves, which may account for their lower survival in winter. Wild fish in the north rapidly accumulated large somatic reserves, which were depleted over the winter and then increased again during the subsequent spring breeding season. In wild southern fish, relatively small reserves accumulated slowly until breeding commenced in the spring. The common-environment comparison of somatic storage patterns revealed a genetic basis for among-population differences in reserve accumulation rates, but no differences in the amount of reserves stored. We conclude that the overwinter depletion of somatic reserves has a significant selective impact on energy accumulation and allocation strategies in seasonal environments. Received: 1 November 1995 / Accepted: 13 September 1996     

Diet, fecundity and egg size in some polyphagous predatory carabid beetles

Egg size was measured at different rates of egg laying in three polyphagous carabid species, known to be useful predators of cereal aphids; the small Bembidion lampros Herbst and the medium-sized Pterostichus cupreus L. and P. melanarius Illiger. Variations in fecundity, as well as the ability of the medium-sized species to also build up fat reserves, were obtained when beetles were subjected to different dietary regimes consisting of aphids, or foods with a lower or higher protein content. Egg size was found to be dependent on the rate of egg laying within a species. A diet of cereal aphids appeared to be adequate for egg production in these polyphagous carabids, but female P. cupreus were unable to build up fat reserves when they ingested aphids contaminated with the aphicide pirimicarb. Beetles were able to devote resources to more and larger eggs (B. lampros), or to larger eggs and/or fat reserves (P. melanarius/P. cupreus) when given access to a carbohydrate-rich food with low protein content. The highest rate of egg laying was obtained when female P. cupreus and P. melanarius were given a more varied diet at frequent intervals; including regular shifts between unsprayed aphids, carbohydrate-rich food and protein-rich maggots. Within the varied diet treatment a negative relationship was obtained between egg size and egg number among similar-sized individuals of P. cupreus and P. melanarius; females producing the largest number also laid the smallest eggs. Egg size affected larval survival, since first instars hatching from large eggs were found to survive longer than those hatching from small eggs. The influence of differences in food intake on reproduction, maintenance metabolism, and survival of fieldinhabiting carabids is discussed.     

Life‐history differences across latitude in common side‐blotched lizards (Uta stansburiana)

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