Host-feeding strategies of parasitoid wasps

Summary Three models of the evolution of host-feeding behaviour in parasitoid wasps are developed. The first assumes that the wasp host feeds purely to obtain resources to mature eggs (limited resource model) while the second assumes that host feeding provides energy for maintenance (pro-ovigenic model). The third model assumes that host feeding provides resources for both maintenance and egg maturation (resource pool model). Two variants of the third model are examined: the first assumes that the risk of mortality is constant and state-independent, the second that resource-depleted individuals suffer a higher risk of mortality. The models are analysed using a combination of stochastic dynamic programming and analytical techniques. The models make different predictions about the relationships between the probability of host feeding and egg load and host density. The available experimental evidence best supports the resource pool model.     

Functional and evolutionary aspects of mouthpart structure in parasitoid wasps

This paper considers specializations in mouthpart structure among parasitoid wasps. I commence with a brief survey of mouthpart specializations (mostly involving the mandibles only) that serve functions other than feeding: facilitating emergence of the parasitoid adult from its place of pupation; facilitating grasping of the partner in mating (phoretic copulation); facilitating excavation and/or protecting vulnerable mouthpart components during host searching; facilitating handling of the host; and facilitating nest excavation and construction. I then consider in detail mouthpart specializations for feeding (mostly involving the labiomaxillary complex), and place them in an evolutionary context. Whereas the digitate labrum of Perilampidae and Eucharitidae and the stoudy setose labrum of chrysolampine Pteromalidae are purported to be devices for filtering pollen grains from nectar, I conclude that they are not a feeding-related specialization whatsoever. I recognize seven functional types of mouthpart specialization relating to the extraction of floral nectar from long, narrow, tubular corollas (‘concealed nectar extraction apparatus’ [CNEA]) (Braconidae, Ichneumonidae, Leucospidae, Chrysididae), and postulate a transformation series for them. An eighth type of CNEA possibly occurs in Scoliidae. No such specializations occur in either Orussoidea, Trigonalyoidea, Megalyroidea, parasitoid Evanioidea, Stephanoidea, Cynipoidea, Proctotrupoidea, Ceraphonoidea or parasitoid Aculeata other than Chrysididae and Pompilidae. From examination of published cladograms I conclude that the evolution of CNEA has occurred several times independendy within the parasitoid Hymenoptera. So far as Ichneumonoidea are concerned, possession of CNEA is an autapomorphy for taxa at least below subfamily level. Possession of CNEA appears to be a synapomorphy for the family Leucospidae (Chalcidoidea) as a whole, and the same applies to the subfamily Parnopinae (Chrysididae). Hitherto not noted in the literature is the strong degree of evolutionary parallelism, with respect to CNEAs, between the Ichneumonoidea (Ichneumonidae, Braconidae) and the Aculeata (Chrysididae, Pompilidae, Vespidae [Vespinae, Masarinae, Eumeminae], Apidae, non-parasitoid Sphecidae). Also, Apocrita and Symphyta have two types of CNEA in common. Functional comparisons are made between the CNEAs of the parasitoids and those of other Hymenoptera. Compared to parasitoid flies, very few parasitoid wasps possess CNEA. Mouthpart specialization for conveying a nuptial gift of nectar or honeydew to the female occurs in the males of thynnine Tiphidae, while in the females of regurgitation feeders there is a trend towards reduction in labiomaxillary components, constituting a specialization for receiving and processing the gift. Mouthpart specialization for pollen feeding occurs in Mutillidae and Scoliidae. No mouthpart specialization for host feeding occurs in any parasitoid wasps, in contrast to parasitoid flies, despite host feeding being more common among the former. Sexual dimorphism in feeding-related mouthpart specializations is rare among parasitoid wasps; where it occurs, both sexes share the same type of CNEA, and the dimorphism is attributable to allometry.     

Sib-mating and sex ratio strategies in scelionid wasps

Abstract. 1. Theoretical models by Hamilton and others predict that the optimal sex ratio (proportion males) for a species should decrease with increasing levels of sib-mating. A test of this hypothesis is made for members of the parasitoid family Scelionidae.
2. Scelionid wasps differ in levels of sib-mating as a consequence of differences in host egg mass size, male—male aggression and female—female aggression.
3. Sex ratios for thirty-one species vary with inferred changes in sib-mating as predicted by the models.
4. Interspecific differences in sex ratio may represent different fvted strategies or different manifestations of a single variable strategy (sex ratio game) in response to parasitoid-produced stimuli.
5. Males and females are assigned non-randomly to egg masses in a manner which ensures mixed broods in the proper proportions for a particular species.     

Influence of adult nutrition on the relationship between body size and reproductive parameters in a parasitoid wasp

Abstract.  1. An important constraint upon life-history evolution in parasitoids is the limit imposed by body size on allocation of limited metabolic resources to different fitness-related physiological functions such as reproduction and survival.
2. The influence of adult nutrition on reproductive and maintenance variables was studied in the synovigenic ectoparasitoid Mastrus ridibundus , and it was determined whether resource allocation to these different functions depends on body size.
3. Over the course of adult life there was a positive relationship between body size and the number of mature eggs in adult females both in the presence and absence of food. However, only in the presence of food did egg maturation rates increase significantly with body size. Starved wasps produced significantly smaller eggs than fed ones, which has not been documented before. Moreover, starved wasps produced fewer offspring than fed wasps, and attacked fewer hosts.
4. The availability of food had a major effect on longevity, with fed females living about 10 times longer than starved ones. There was also a positive relationship between body size and longevity. In starved wasps, this relationship was the same both in the presence and absence of hosts, but in fed wasps there was a positive relationship between body size and longevity in the absence of hosts only. Allocation to initial eggs relative to lifetime progeny production did not decline with body size.
5. The data reveal that in M. ridibundus the trade-off between maintenance and reproduction varies with life expectancy.     

Life-history strategies of a freshwater snail in response to stream permanence and predation: balancing conflicting demands

Summary Life-history parameters for the freshwater snail Physella virgata virgata were estimated in temporary and permanent streams with and without crayfish (known snail predators). Snails from the permanent stream with crayfish exhibited higher age and size at first reproduction, as well as higher size and age at death, compared to snail populations from both temporary streams and the permanent stream without crayfish. Life-history patterns of snails from the permanent and temporary streams without crayfish were indistinguishable, with small sizes at first reproduction and at death, as well as lower age at first reproduction and at death. The snail population from the temporary stream with crayfish showed an intermediate life-history pattern. The results suggest that snail life-history patterns vary with both predation pressure and habitat stability, exhibiting phenotypically plastic responses to the variables.     

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.     

Dynamic egg maturation strategies in an aphid parasitoid

Abstract.  Females of the parasitoid Aphelinus albipodus both lay more eggs on younger stages of their aphid host, Aphis glycines , and contain more mature eggs in their ovaries when held with these younger host stages. This suggests that egg maturation is more rapid in the presence of younger host stages. Three factors explaining the difference in the egg loads of A. albipodus females exposed to various host stages are examined. These are (i) the number of host-feeding meals; (ii) the number of eggs laid; and (iii) the host stage utilized. Together, these factors explain 69% of the variance in A. albipodus egg load. The number of host-feeding meals taken by females is a strong predictor of egg load. More host meals are taken on young hosts, suggesting that host feeding contributes to the trend of faster egg maturation in the presence of younger hosts. Host stage has a strong impact on egg load even when the effect of host feeding is accounted for. There is no evidence for an effect of the oviposition rate on egg load. The results indicate that egg maturation by A. albipodus is dynamic; females mature eggs faster when in the presence of preferred hosts. It is hypothesized that this allows A. albipodus females to more closely match their reproductive effort to reproductive opportunities.     

The evolution of host use and unusual reproductive strategies in Achrysocharoides parasitoid wasps

We studied host selection and exploitation, two crucial aspects of parasite ecology, in Achrysocharoides parasitoid wasps, which show remarkable host specificity and unusual offspring sex allocation. We estimated a molecular phylogeny of 15 Achrysocharoides species and compared this with host (plant and insect) phylogenies. This tri-trophic phylogenetic comparison provides no evidence for cospeciation, but parasitoids do show phylogenetic conservation of the use of plant genera. Patterns of sequence divergence also suggest that the parasitoids radiated more recently (or evolved much faster) than their insect hosts. Three main categories of brood production occur in parasitoids: (1) solitary offspring, (2) mixed sex broods and (3) separate (split) sex broods. Split sex broods are very rare and virtually restricted to Achrysocharoides, while the other types occur very widely. Our phylogeny suggests that split sex broods have evolved twice and provides evidence for a transition from solitary to mixed sex broods, via split sex broods, as predicted by theory.     

Spermatogeny as a life-history index in parasitoid wasps

Reproduction is a major life-history trait but it has been studied mostly in relation to female reproductive effort. Recently, an ovigeny index using the proportion of oocytes ready to be oviposited at eclosion has been proposed for female insect parasitoids. Here, we propose a spermatogeny index for male parasitoid wasps. Prospermatogenic species have an index of 1, have all their spermatozoids mature at emergence and do not produce more later in life. At the other end of the spectrum, synspermatogenic species have no spermatozoids at emergence and produce them later in life. The level of spermatogeny should be linked to several other life-history parameters such as longevity, size, nutrition, distribution of mating opportunities and dispersion before and after mating. Data presented for some parasitoid species support the presence of variability in this male life-history parameter.     

Life-history variation within a taxon: a comparative analysis of birds and mammals

Most studies on life-history evolution discuss the necessity of distinguishing between extrinsic and intrinsic sources of variability in life-history traits. I use log/log plots of yearly neonate production in daugters (b) versus adult mortality (Ma) for 75 bird species and 88 mammal species to compare graphically life-history "fields" arranged by these selective forces along a "slow-fast continuum". Under the assumptions of steady-state and linear relationship between adult mortality and reproductive effort, as well as between juvenile survival and relative neonate weight, it is possible to place additional axes in the two-dimentional plot, and to predict covariations among demographic and individual growth traits. The functional regression analysis shows, that the assumptions are completely fulfilled, at least for birds, but mammals show nonlinear relationship between adult mortality and reproductive effort. This can be explained by peculiarities of metabolism and parental care in small mammals with high reproductive output. Hence, for birds the axis of relative neonate weight approximately coincides in direction with the juvenile survivorship axis, but this is not a case for mammals. In both taxa, the relative neonate weight is an invariant in relation to fecundity and adult mortality (but not in relation to adult body weight). This important feature, together with other intrinsic (energetic and phylogenetic) constraints, explains well-documented close covariations among traits, even when the effect of body size is factored out. It is argued that life-history and body size variations in birds and mammals mainly depend on a pattern of temporal resource deficiency, although this impact cannot be separated from that of extrinsic juvenile mortality.     

Taxonomy of parasitoid wasps in China: An overview

The parasitoid Hymenoptera are one of the most important groups of natural enemies of agriculture and forestry pests and have been used as biological control agents in IPM programs for a long time. The systematic research on parasitoids and their associations with hosts lays a solid base for biological control of pests. Here we summarize the taxonomic studies undertaken on the parasitoid wasps in China in the last eight decades. At present about 48 families in 12 superfamilies of parasitoid Hymenoptera are known in China, of which the majority of the families have been studied to some extent while a number of them are still poorly studied. Around 6000 species of 32 families which dealt with in this paper are known in China, and some of them have been successfully and widely used in the existing biological control while others are potentially useful in future biocontrol program. This overview provides the international audience a general idea about the current state of the systematic study of parasitoid Hymenoptera conducted in China, the known species of parasitoids and the native and introduced species used in biocontrol in China.     

REVIEW: The evolution of polyembryony in parasitoid wasps

Polyembryony has evolved independently in four families of parasitoid wasps. We review three main hypotheses for the selective forces favouring this developmental mode in parasitoids: polyembryony (i) reduces the costs of egg limitation; (ii) reduces the genetic conflict among offspring; and (iii) allows offspring to adjust their numbers to the quality of the host. Using comparative data and verbal and mathematical arguments, we evaluate the relative importance of the different selective forces through different evolutionary stages and in the different groups of polyembryonic wasps. We conclude that reducing the cost of egg limitation is especially important when large broods are favoured. Reducing genetic conflict may be most important when broods are small, thus might have been important during, or immediately following, the initial transition from monoembryony to polyembryony. Empirical data provide little support for the brood‐size adjustment hypothesis, although it is likely to interact with other selective forces favouring polyembryony.     

Molecular analysis of parasitoid linkages (MAPL): gut contents of adult parasitoid wasps reveal larval host

Metamorphosing insects often have complex and poorly known life histories. In particular, what they feed on during their larval stages remains unknown for the vast majority of species, and its documentation only results from difficult and time-intensive field observations, rearing or dissections. Through the application of a DNA analysis of gut contents in adult parasitoid wasps, we were able to selectively sequence a diagnostic DNA marker that permitted the identification of the host used by these wasps during their larval stages. By reproducing these results in species with different life histories, we excluded other potential sources of host DNA, confirming that after ingestion by the parasitoid larva the host DNA can persist through metamorphosis in the abdominal contents of the adult wasp. Our discovery considerably extends the applicability of molecular analysis of gut contents by enabling the documentation of food used by insects during their larval stages and thus increasing the accuracy and precision of food web studies. The 24% success rate of our approach is surprisingly high considering the challenging context for host DNA preservation, and we discuss the factors possibly affecting this rate. We propose molecular analysis of parasitoid linkages (MAPL) as a new method to document host-parasitoid associations at a faster pace and with unrivalled precision. Because of the key regulatory role of parasitoid wasps in ecosystems, which makes them the most commonly used biological control agents, MAPL will have immediate applications in both basic and applied biological sciences.     

Egg resorption behaviour by the solitary egg parasitoid Anaphes nitens under natural conditions

We investigated under outdoor conditions and inside a climate chamber: (i) whether Anaphes nitens Girault (Hymenoptera: Mymaridae), an egg parasitoid of the Eucalyptus snout beetle, Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae), experienced egg resorption, and (ii) how various treatments (location, food, and/or host supply) and body size influenced egg load, egg resorption, fecundity, and longevity. One‐day‐old females were mated and randomly assigned to five groups: (A) honey + hosts, (B) water + hosts, (C) only honey, (D) only water, and (E) control females killed at emergence. We compared the egg load of the newly emerged females, which represent the control group (egg load = ovarian eggs present at emergence), with the lifetime egg load (i.e., ovarian eggs + emerged offspring + not emerged offspring) of the females with various host and diet treatments, by dissection of the ovaries to find evidence of egg resorption. All groups reared outdoors had fewer eggs than the control, while indoors there was no significant difference. Outdoors, starved but host‐provided wasps (B) experienced the highest reduction of the lifetime egg load (51%). Groups without access to food (B + D) resorbed more eggs than groups provided with honey (A + C). Females with honey and hosts (A) had the highest lifetime fecundity, but those with water and hosts (B) showed a higher daily realized fecundity. Host‐deprived females with access to food (C) attained the longest lifespan. Our results suggest that under stress conditions, such as low temperature and food shortage, A. nitens females practice egg resorption, probably to save energy.