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Parasitoids are insects whose females lay their eggs in or on other invertebrates (mostly other insects) and whose larvae feed on the host and eventually kill it. The number of eggs that a female parasitoid deposits during her lifetime is determined by interactions among three processes: the number of suitable hosts that are encountered, the number of eggs that are matured over the female’s life span, and behavioural manipulation of the oviposition rate. Environmental stochasticity is expected to prevent exact matching of egg and host availability (Rosenheim 1996), but there is some evidence that natural selection adjusts egg production characteristics to approach the expected rate of host encounter (Price 1975; Rosenheim 1996; Sevenster, Ellers & Driessen 1998). Behavioural plasticity also allows parasitoid females to improve the match between host and egg availability (Charnov & Skinner 1984; Mangel & Heimpel 1998).
Parasitoid egg production traits that are potentially important in improving congruence between egg and host availability include: the total number of stem line oocytes (known as oogonia; their number sets the maximum potential fecundity), the maximum number of mature (i.e. fully chorionated) eggs that can be stored within the ovaries at a given time, the rate of egg maturation, the size of mature eggs and the capacity for, and rate of, egg resorption (Price 1975; Jervis & Kidd 1986). An important outcome of interactions among these characteristics is that, of the total number of oocytes a female carries, the fraction of the maximum potential lifetime egg complement that is mature when she emerges into the environment varies greatly among parasitoid taxa. Flanders (1950) classified parasitoid wasps that have all or nearly all of their eggs mature prior to the start of oviposition as ‘pro-ovigenic’ and those that continue to mature eggs throughout their reproductive life as ‘synovigenic’. This distinction continues to be widely applied in the literature on parasitoids, and recently several models have contrasted the effects of pro-ovigeny and synovigeny both on the evolution of parasitoid life-history strategies (Chan & Godfray 1993; Hunter & Godfray 1995; West, Flanagan & Godfray 1999; Ellers, Sevenster & Driessen 2000; Rosenheim 2000; Rosenheim, Heimpel & Mangel 2000) and on host–parasitoid population dynamics (Kidd & Jervis 1989; Shea et al. 1996).
While Flanders’ concept has been useful, it also glosses over much of the diversity found in parasitoid egg maturation strategies, particularly among synovigenic species. Also, it was formulated before the development of modern life-history theory, particularly that predicting a trade-off between reproduction and life span (Roff 1992; Stearns 1992). Here, we review and explore in more detail the diversity in egg maturation patterns among the parasitoid Hymenoptera, and place it in the context of life history theory in general and of that pertaining specifically to the reproductive strategies of parasitoids. Our main goal is to test a series of hypotheses that relate ovigeny to various life-history traits in parasitoids. We briefly discuss each hypothesis in turn.
A continuum of ovigeny is likely to exist, in which species can range from pro-ovigenic (all eggs are mature at emergence), through weakly synovigenic (most eggs are mature at emergence) to extremely synovigenic (no eggs are mature at emergence) (Jervis & Copland 1996
; Quicke 1997
) (note that our definition of pro-ovigeny is more conservative than that of Flanders). This prediction is based on published data on egg maturation patterns which tentatively indicate that there may be such a continuum.
Across parasitoid wasp taxa, life span should be negatively correlated with the proportion of oocytes mature upon emergence, and so pro-ovigenic wasps should be shorter-lived than synovigenic ones (Flanders 1950
). Life-history theory predicts that a concentration of ‘reproductive effort’ towards the start of adult life should incur a life-span cost. Recently, Ellers & van Alphen (1997)
provided evidence that an inverse relationship exists between life span and the proportion of oocytes mature at emergence among geographical strains of the parasitoid wasp Asobara tabida
Host feeding (i.e. the consumption of host haemolyph and/or tissues by adult parasitoids) should be confined to synovigenic species, as suggested by Flanders (1950)
(see also hypothesis 4).
Host feeding should be associated with a relatively low proportion of oocytes mature upon female emergence. The reasoning behind this is as follows: whereas female pro-ovigenic and weakly synovigenic wasps presumably require nutrients more for maintenance purposes, strongly synovigenic wasps need to fuel both maintenance and reproduction. Trehalose and proline, both of which can occur in significant amounts in host blood, can potentially be used for somatic maintenance in the broad sense (Gilbert & Jervis 1998
). Host tissues and blood are a rich source of egg production nutrients: proteinaceous materials, fats and sugars and also essential vitamins and salts that are either scarce or absent in other foods (Jervis & Kidd 1986
; Heimpel & Collier 1996
; Rivero & Casas 1999a
). At least some synovigenic, host-feeding species can allocate to reproduction, over a long time period (~2 weeks in Dinarmus basalis
Rondani), nutrients originally acquired from a single meal taken early on in life (Rivero & Casas 1999a
The production of yolk-deficient (hydropic) eggs should be associated with a higher proportion of eggs mature upon female emergence than the production of yolk-rich (anhydropic) eggs (see hypotheses 6, 7 and 8).
Egg resorption capability should be concentrated among anhydropic egg-producers, as hydropic eggs contain little or no yolk for the female to salvage.
Egg resorption capability should be associated with a relatively low proportion of oocytes mature upon female emergence. Resorption usually precludes oviposition and can be a time-consuming process (Jervis & Kidd 1986
), so it is likely to be practised by longer-lived species, long life span being a trait predicted to be associated with a low proportion of oocytes mature upon emergence (see hypothesis 2).
Egg maturation strategy should be linked to the mode of parasitism. Two alternative, supposedly divergent (Mayhew & Blackburn 1999
) life-history strategies are widely recognized as occurring among parasitoids with respect to development mode: ‘koinobiosis’ in which the host continues to develop, grow (if attacked as a larva), reproduce (if attacked as an adult), and remain active after attack, and ‘idiobiosis’ in which the host does not continue to develop, grow or remain active after attack (Askew & Shaw 1986
; Shaw & Huddleston 1991
). Several authors (Askew 1975
; Force 1975
; Price 1975
; Blackburn 1991a, 1991b
) have proposed that divergent suites of traits are associated with koinobiosis and idiobiosis, and that natural selection operates on the life history strategies of the two sorts of parasitoids to magnify the initial differences. This view was summarized by Godfray (1994)
as the ‘dichotomous hypothesis’. Space does not permit a detailed discussion of all the life-history parameters and the various selection pressures acting upon them (see the aforementioned references); we confine ourselves here to discussion of the parameters we consider to be most relevant to ovigeny. Mayhew & Blackburn (1999)
, using phylogeny-based statistical techniques applied to a literature database, established that koinobioints, compared with idiobionts, have a shorter adult life span and produce smaller (= yolk-poor) eggs, and have a higher realized fecundity and a higher maximum rate of oviposition.
We hypothesize that ovigeny index may be linked to development mode for the following reasons: (i) a higher realized fecundity can be achieved by producing smaller (hydropic) eggs – a recognized trade-off (Godfray 1994); (ii) female adult koinobionts are shorter-lived than those of idiobionts (Mayhew & Blackburn 1999), and correlated with this should be a higher proportion of oocytes mature upon emergence (hypothesis 2); (iii) koinobiosis is supposed to select for a higher oviposition rate (including a minimal, if any, preovi-position period) which can be achieved by a tendency towards pro-ovigeny (Blackburn 1991b); (iv) koinobionts spend longer as pupae compared with idiobionts (Blackburn 1991a), and this ought to allow more time for oocytes to develop prior to female emergence.
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Based on the various types of information used, we were able to identify the egg maturation type (pro-ovigenic or synovigenic) shown by 638 species belonging to 28 families within the ‘Parasitica’ and the Aculeata of the order Hymenoptera (Table 1). Of these, the vast majority (98·12%, n = 626) are synovigenic, while only 12 species (1·88%) are unambiguously pro-ovigenic. We encountered little difficulty in categorizing the majority of species we obtained information on, and where species had been previously categorized, there was little disagreement.
Table 1. Parasitoid wasp families represented in our sample, their size, and the numbers of pro- and synovigenic species we categorized within each
|Superfamily/family||Family size||Number of species in our sample||Number of ‘strictly’ pro-ovigenic species||Number of synovigenic species|
|Trigonalyoidea|| || || || |
| Trigonalyidae|| 70|| 4|| 0|| 4|
|Playgastroidea|| || || || |
| Platygastridae|| 987|| 2|| 1|| 1|
| Scelionidae|| 2 768|| 3|| 0|| 3|
|Proctotrupoidea|| || || || |
| Diapriidae|| 2 028|| 1|| 0|| 1|
|Chalcidoidea|| || || || |
| Aphelinidae|| 1 118|| 25|| 1|| 24|
| Chalcididae|| 1 455|| 5|| 0|| 5|
| Elasmidae|| 212|| 2|| 0|| 2|
| Encyrtidae|| 3 700|| 20|| 1|| 19|
| Eucharitidae|| 383|| 1|| 1|| 0|
| Eulophidae|| 3 965|| 11|| 0|| 11|
| Leucospidae|| 132|| 2|| 0|| 2|
| Mymaridae|| 1 402|| 6|| 6|| 0|
| Perilampidae|| 280|| 2|| 0|| 2|
| Pteromalidae|| 3 368|| 16|| 0|| 16|
| Signiphoridae|| 77|| 1|| 0|| 1|
| Torymidae|| 966|| 1|| 0|| 1|
| Trichogrammatidae|| 795|| 8|| 0|| 8|
|Cynipoidea|| || || || |
| Charipidae|| 1 200|| 1|| 0|| 1|
| Eucoilidae|| 1 000|| 4|| 2|| 2|
|Ichneumonoidea|| || || || |
| Ichneumonidae||15 000||411|| 0||411|
| Braconidae||10 000|| 76|| 0|| 76|
|Chrysidoidea|| || || || |
| Bethylidae|| 2 000|| 7|| 0|| 7|
| Dryinidae|| 850|| 3|| 0|| 3|
|Vespoidea|| || || || |
| Mutillidae|| 5 000|| 4|| 0|| 4|
| Pompilidae|| 4 000|| 11|| 0|| 11|
| Scoliidae|| 300|| 5|| 0|| 5|
| Tiphiidae|| 1 500|| 2|| 0|| 2|
|Apoidea|| || || || |
| Sphecidae|| 7 700|| 4|| 0|| 4|
We examined the numbers of pro-ovigenic and synovigenic species in each family of parasitoid wasps, in relation to the size of that family (Table 1). Data on family sizes were taken from Gaston (1991), Gauld & Bolton (1988), Johnson (1992), Noyes (1990 and personal communication) and Vlug (1993). Six families from three superfamilies contained pro-ovigenic species (Platygastridae, Eucoilidae, Eucharitidae, Mymaridae, Pteromalidae and Aphelinidae, Table 1). We took the proportions of pro-ovigenic and synovigenic species in our sample of each family to be representative of that family. The grand mean proportion, weighted by the estimated number of described species in each family, indicates that we ought to have found 27 pro-ovigenic and 611 synovigenic species (4·23% and 95·77%, respectively), a significant difference compared with our sample (χ2 = 8·33, P < 0·005). Thus, even accounting for taxonomic (family) bias in our sample, pro-ovigeny is rare among parasitoid wasps. Of course, the assumption that the proportions of the different ovigeny types per family sample are representative is questionable (although accounts of oviposition behaviour suggest it is probably correct for the Eucharitidae, see Clausen 1940, 1941), and several of our family samples (e.g. the Ichneumonidae) are certainly strongly biased towards particular subfamilies. Only a more extensive survey can provide a conclusive answer as to the real representation of the different ovigeny types among parasitoid wasps. Quantitative information on ovigeny was available for only a small proportion (≈ 10%) of the 638 species that we established to be pro-ovigenic or synovigenic. Table 2 presents ovigeny indices for these 67 species. The data strongly support previous suggestions (Jervis & Copland 1996; Quicke 1997) that there is a continuum of ovigeny from an index of 0 (extreme synovigeny) to an index of 1 (pro-ovigeny) (hypothesis 1) Fig. 1). Our subsample of synovigenic species clearly had a non-normal distribution of ovigeny indices (Fig. 1; Shapiro–Wilkes’W-test for normality: P < 0·001), with 35% of species emerging with no mature eggs (index = 0), a median value of 0·05 and positive skewness (g1 = 0·85). The mean index for synovigenic species was 0·22 with a variance of 0·07. The maximum index value for a synovigenic species was 0·75. The gap between 0·75 and 1 in Fig. 1 may be attributed to undersampling and/or evolutionary instability of ovigeny values in that range, but note that there are three species (not plotted) with an index of ‘~1’.
Thirty-four independent comparisons between life span and ovigeny index were available for testing hypothesis 2. These revealed a significant negative relationship between life span and the proportion of oocytes mature upon adult emergence (Fig. 2) (PT: line forced through the origin, slope = − 0·292, t33 = −4·51, P < 0·0001; TT: slope = −0·375, F1,39, P < 0·0001). Ovigeny index accounted for 38% of the variation in life span, correcting for phylogeny. Hierarchical anova revealed that the largest percentage of the variation in life span occurred at the level of the species within the genus (46·4%) and in ovigeny index at the level of the family within the superfamily (51·4%). The smallest percentage of the variation in both life span and ovigeny index was at the level of the genus within the family (9·4% and 4·7% respectively).
Figure 2. The relationship between life span and ovigeny index (a) as revealed by a method that takes account of the fact that trait values may not be independent of phylogeny, and (b) by a traditional method of regression. The former analysis was undertaken using Harvey & Pagel’s (1991) method of independent comparisons which assesses a comparative relationship by analysing the differences between variable scores in immediately adjacent branches of the phylogenetic tree, rather than the raw variable scores. This is based on the logic that the differences must have evolved after the branches diverged, thereby eliminating all similarity due to common descent. Note that the number of data points in (a) is less than the number of species on which the analysis is based. Differences in trait may, in principle, be scaled by the branch lengths, but we could not do this as too many branch lengths are unknown.
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We examined whether any life-history variable(s) on which we had gathered data accounted for the residuals in the relationship between life span and ovigeny. We could use only traditional statistical techniques, as statistical power was too low using a phylogeny-based analysis. When the effect of ovigeny index on life span was removed, residual life span was not significantly related to either female feeding habit, egg type, egg resorption capability, larval development mode or female fecundity.
Intraspecific variation was not included in the above analysis, but geographical populations (Asobara tabida SIN and KOS strains) and subsamples of a population (Trichogramma nubilale Ertle & Davis large and small wasps) that had the largest proportion of oocytes mature upon emergence also had the shortest life span (Ellers & van Alphen 1997; Olson & Andow 1998).
Comparing the life span of pro-ovigenic vs. synovigenic parasitoids (i.e. testing Flanders’ 1950 observation that the latter are longer-lived, hypothesis 2), we found that the life span of synovigenic species (mean ± SE: 25·8 ± 2·2 days, n = 63) is indeed significantly greater than that of pro-ovigenic species (9·0 ± 1·5 days, n = 10) (PT: paired t6 = 1·89, P = 0·027; TT: t71 = 6·25, P < 0·0001).
Although host feeding has been unequivocally recorded in many synovigenic species (Jervis & Kidd 1986) it is unclear whether it is actually confined to synovigenic wasps (hypothesis 3). The pro-ovigenic aphelinid Eretmocerus sp. displays behaviour suggestive of host feeding: females use the ovipositor to sting and then probe the whitefly host close to the latter’s anal region, and they then apply their mouthparts to the wound. However, it needs to be established whether they consume mainly the host’s blood or mainly the honeydew contained in the host’s hind gut (if they take mainly honeydew, they are very likely to do so from the gut rather than from elsewhere, because the hosts – atypically for Sternorrhynha – jettison their honeydew well away from the patch; M.J.W. Copland, personal communication).
Host feeding species tend on average to have a lower ovigeny index (hypothesis 4) (host feeders: 0·088 ± 0·066 [n = 15] vs. others: 0·479 ± 0·079 [n = 27]) and this difference is significant according to the traditional analysis (TT: t40 = −3·81, P = 0·0002) but not the phylogeny-based analysis (PT: paired t3 = −1·00, P > 0·10). Note that the data set included Eretmocerus sp. as a host feeder. Because there is some doubt as to whether this species mainly consumes host materials or honeydew, we tested hypothesis 4 again, this time coding Eretmocerus sp. as a parasitoid wasp which does not consume host tissues or blood. Again, the phylogeny-based test failed to reveal an association (PT: paired-t, t4 = 0·47, P > 0·2) whereas the traditional test did (TT: one-tailed, t40 = 3·72, P = 0·0003). However, it should be noted that in both of the above phylogeny-based analyses the number of transitions in the tree was low (i.e. statistical power was low). The results of similar analyses, based on a taxonomically more extensive data set, could well stand in favour of hypothesis 4.
The data unequivocally support hypothesis 5, which argues that producers of hydropic eggs have on average a significantly higher ovigeny index than producers of anhydropic eggs (0·585 ± 0·070 [n = 30] vs. 0·108 ± 0·062 [n = 22]) (PT: paired t4 = 2·52, P = 0·043; TT: t49 = 4·91, P < 0·00001). (Note that whereas, according to the dichotomous hypothesis, hydropic egg production is considered to be a means of maximizing fecundity [see hypothesis 8], we found no statistically significant link between ovigeny index and fecundity.)
As predicted (hypothesis 6), the ability to resorb eggs was recorded mainly (indeed, only) from anhydropic egg-producers, which themselves appear to be confined to synovigenic species (note that anhydropic egg-producers include species that do not host feed). Also as predicted (hypothesis 7), egg resorbers have a significantly lower ovigeny index than non-resorbers (0·022 ± 0·009 [n = 12] vs. 0·575 ± 0·069 [n = 28]) (PT: paired t4 = 2·54, P = 0·032; TT: t38 = 7·92, P < 0·00001).
Koinobionts tend to have on average a higher ovigeny index than idiobionts (hypothesis 8) (0·473 ± 0·081 [n = 25] vs. 0·313 (0·076 [n = 31]), and this difference is significant according to the phylogeny-based analysis but not according to the traditional analysis (PT: one-tailed paired t6 = 2·56, P = 0·011; TT: one-tailed t53 = 1·48, P = 0·072). As Godfray (1994) notes, the dichotomous hypothesis pertains mainly to parasitoids attacking host larval stages. Although Mayhew & Blackburn (1999) found a strong degree of support for the hypothesis in an analysis that encompassed parasitism of a broader array of host stages, we chose to test hypothesis (8) further, using the subset of our database containing only parasitoids of larval stage hosts. Again, koinobionts tend on average to have a higher ovigeny index than idiobionts (0·477 ± 0·093 [n = 19] vs. 0·008 ± 0·005 [n = 11]) but in this case the difference is statistically very highly significant according to the traditional analysis and falls just short of being significant according to the phylogeny-based analysis (PT: one-tailed paired t2 = 2·83, P = 0·0527; TT: one-tailed t28 = 5·08, P = 0·000065). Taking the aforementioned results as a whole, it is reasonable to conclude that hypothesis 8 is upheld, i.e. ovigeny is linked to development mode. Support for this stance comes from the results of ancillary tests we conducted specifically to establish whether the dichotomous hypothesis holds when tested against our data set. Using our data for parasitoids of larval stages, the trends for two major life-history variables covered by the dichotomous hypothesis (egg type, life span) are all in the predicted direction: towards hydropic egg production in koinobionts (one-tailed Fisher’s exact test, PT: n = 11, P = 0·175; TT: n = 54, P = 0·0006) and towards a shorter life span in koinobionts (PT: paired-t, t4 = 2·95, P = 0·021; TT: one-tailed t, t25 = 2·47, P = 0·022). (There were insufficient data for fecundity to be considered.) Ovigeny therefore appears to be the final, major piece in the jigsaw of life-history traits forming the dichotomous hypothesis. However, we lacked sufficient information to be able to control for the effects of major correlates (e.g. life span and egg type) of ovigeny index and development mode, and therefore see whether the observed relationship still holds. Given a better data set, future investigators might explore this using phylogenetic multiple regression techniques (see Mayhew & Blackburn 1999).
In summary, despite the potentially confounding effects of using a data set derived from different studies carried out under different conditions by different researchers, we found support for most of the hypotheses tested.
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We thank the following who provided valuable advice and/or information: Jacques van Alphen, Hasan Basibiyuk, Robert Belshaw, Tim Blackburn, Jerome Casas, C.C. Chien, Tim Collier, Mike Copland, Jim Cronin, Jacintha Ellers, Mike Fitton, Alan Grafen, Ian Hardy, John Heraty, Hefin Jones, Arthur Kopelman, Jana Lee, Suzanne Lewis, Peter Mayhew, Nick Mills, John Noyes, Kazuro Ohno, Susan Opp, Gabriela Perez-Lachaud, Craig Phillips, Andrew Polascek, Donald Quicke, Peter Randerson, Jay Rosenheim, Cetin Sengonça, Mark Shaw, Christine Taylor, Sujaya Udayagiri, Felix Wäckers, Gimme Walter and Susan Weller. We dedicate this paper to the memory of Stanley Flanders, in recognition of his seminal contributions to parasitoid wasp biology.