Phylogeny of the platygastroid wasps (Hymenoptera) based on sequences from the 18S rRNA, 28S rRNA and cytochrome oxidase I genes: implications for the evolution of the ovipositor system and host relationships

The Platygastroidea are a diverse group of mostly small to tiny wasps, the common biology for which is endoparasitism of insect and spider eggs. No analytically‐based phylogeny exists for the superfamily, and the current suprageneric classification is flawed in part because of its reliance on homoplasious and pleisiomorphic morphological characters. To determine platygastroid relationships as a basis for investigating host and ovipositor evolution, phylogenies of > 70 in‐group species (representing 55 genera) were reconstructed by parsimony and Bayesian methods using three molecular markers; the mitochondrial cytochrome oxidase I and the nuclear genes 28S and 18S rRNA. The results strongly support the monophyly of the superfamily and one of the two families, Platygastridae, but the Scelionidae are most likely polyphyletic. However, within the Scelionidae, there is a well supported ‘main scelionid clade’ that contains the majority of genera assigned to the family. At the subfamilial level, both putative subfamilies of Platygastridae, the Platygastrinae, and Sceliotrachelinae, are likely to be polyphyletic. Within the Scelionidae, both the Teleasinae and Telenominae are monophyletic, but the Scelioninae is clearly not so. The current tribal classification for the Scelionidae is in need of major reassessment because no tribes, with the exception of the Scelionini s.s., were found to be monophyletic. Further illustrating the problems associated with the current classification is the nonmonophyly of a number of genera, namely Opisthacantha Caloteleia, Telenomus, Trimorus, Teleas and Idris. Analysis of ovipositor evolution in the superfamily revealed that the Ceratobaeus‐type ovipositor system is ancestral; however, this trait was lost prior to the evolution of the main scelionid clade, for which the Scelio‐type ovipositor system is ancestral and defines a mostly paraphyletic assemblage. Ancestral state analysis indicates that the Ceratobaeus‐type ovipositor was subsequently re‐evolved in the main scelionid clade, representing a possible contradiction of Dollo’s law. Previously, the tribal placement has been used to predict the host associations of genera for which host data were unavailable. However, the fact that most tribes are not monophyletic throws into doubt any such speculation based on the current classification. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91 , 653–669.     

Field collection of egg parasitoids of Pentatomidae and Scutelleridae in Northwest Italy and their efficacy in parasitizing Halyomorpha halys under laboratory conditions

The invasion of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) has caused severe economic damage in crops in North America and Europe, motivating research to identify its natural enemies, both in native and invaded areas. In its Asian native range, the main natural enemies are egg parasitoids, among which the most effective are Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in China and Japan, respectively. In Europe, biology, host range, and impact of most native scelionid species are not well‐known. The present study aimed to investigate (1) presence and abundance of scelionid species that parasitize native Pentatomidae and Scutelleridae eggs in Northwest Italy, and (2) their ability to develop on H. halys eggs. During 4‐year field surveys, egg masses were collected and reared until bug nymph or adult parasitoid emergence. Then, the obtained scelionid females were tested for their ability to parasitize H. halys eggs in laboratory no‐choice experiments. Egg masses of all collected bug species were parasitized, and Telenomus spp. (Hymenoptera: Scelionidae), Trissolcus belenus (Walker), and Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) were the most common parasitoids. In the laboratory, Trissolcus kozlovi Rjachovskij was the only species to significantly produce offspring from fresh H. halys eggs, whereas all tested Trissolcus species significantly induced host egg abortion (non‐reproductive effects). This study provides knowledge of the parasitoid species associated with native bugs, and represents a starting point to investigate the intricate interactions between native and exotic parasitoids recently found in northern Italy. These egg parasitoids could potentially be effective biocontrol agents of H. halys.     

Fitness of Encarsia sophia (Hymenoptera: Aphelinidae) parasitizing Trialeurodes vaporariorum and Bemisia tabaci (Hemiptera: Aleyrodidae)

Abstract Fitness and efficacy of Encarsia sophia (Girault & Dodd) (Hymenoptera: Aphelinidae) as a biological control agent was compared on two species of whitefly (Hemiptera: Aleyrodidae) hosts, the relatively smaller sweetpotato whitefly, Bemisia tabaci (Gennadius) biotype ‘B’, and the larger greenhouse whitefly, Trialeurodes vaporariorum (Westwood). Significant differences were observed on green bean (Phaseolus vulgaris L.) in the laboratory at 27 ± 2°C, 55%± 5% RH, and a photoperiod of 14: 10 h (L: D). Adult parasitoids emerging from T. vaporariorum were larger than those emerging from B. tabaci, and almost all biological parameters of E. sophia parasitizing the larger host species were superior except for the developmental times of the parasitoids that were similar when parasitizing the two host species. Furthermore, parasitoids emerging from T. vaporariorum parasitized more of these hosts than did parasitoids emerging from B. tabaci. We conclude that E. sophia reared from larger hosts had better fitness than from smaller hosts. Those from either host also preferred the larger host for oviposition but were just as effective on smaller hosts. Therefore, larger hosts tended to produce better parasitoids than smaller hosts.     

Phoresy ofTelenomus sp. (Scelionidae: Hymenoptera), an egg parasitoid of the tussock mothEuproctis taiwana

The phoretic relationship between the egg parasitoidTelenomus sp. cf.euproctidis Wilcox and its host the tussock mothEuproctis taiwana was studied in Okinawa, Japan. One third of the female moths studied in the field carried female parasitoid adults. No male moths carried parasitoids. Parasitoids were observed only in the anal tuft of the moth. Laboratory observation revealed that most of the parasitoids left the body of the moth at the time of the first oviposition of their host and proceeded to lay eggs on the moth egg masses.     

In vitro rearing of Ooencyrtus nezarae (Hymenoptera: Encyrtidae), an egg parasitoid of Riptortus pedestris (Hemiptera: Alydidae)

Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) is a polyphagous egg parasitoid of various true bugs, including Riptortus pedestris (Fabricius) (Hemiptera: Alydidae), a major pest of soybean and fruit trees in northeastern Asia. This study was conducted to develop artificial host eggs containing insect haemolymph for mass rearing of O. nezarae. The haemolymph of Chinese oak silkworm (Antheraea pernyi Guérin-Méneville) pupae was found to be most suitable for artificial eggs for the complete development of O. nezarae. Among 764 parasitoid eggs laid in artificial eggs, 49.2% successfully developed to adult parasitoids. The developmental time in artificial eggs was delayed by 3–5 days relative to that observed in natural host eggs; however there was no significant difference in the length of hind tibia between adults that emerged from artificial and natural host eggs. Moreover, new generations that emerged from artificial eggs reproduced on all egg types offered (either natural or artificial eggs). We propose that the artificial eggs developed herein can therefore be an effective means for mass rearing O. nezarae.     

Morphology agrees with molecular data: phylogenetic affinities of Euptychiina butterflies (Nymphalidae: Satyrinae)

Euptychiina is the most species‐rich subtribe of Neotropical Satyrinae, with over 450 known species in 47 genera (14 monotypic). Here, we use morphological characters to examine the phylogenetic relationships within Euptychiina. Taxonomic sampling included 105 species representing the majority of the genera, as well as five outgroups. A total of 103 characters were obtained: 45 from wing pattern, 48 from genitalia and 10 from wing venation. The data matrix was analysed using maximum parsimony under both equal and extended implied weights. Euptychiina was recovered as monophyletic with ten monophyletic genera, contrasting previous DNA sequence‐based phylogenies that did not recover the monophyly of the group. In agreement with sequence‐based hypotheses, however, three main clades were recognized: the ‘Megisto clade’ with six monophyletic and three polyphyletic genera, the ‘Taygetis clade’ with nine genera of which three were monophyletic, and the ‘Pareuptyhia clade’ with four monophyletic and two polyphyletic genera. This is the first morphology‐based phylogenetic hypothesis for Euptychiina and the results will be used to complement molecular data in a combined analysis and to provide critical synapomorphies for clades and genera in this taxonomically confused group.     

Seasonal phenology and stage-specific parasitism of the apple ermine moth, Yponomeuta malinellus Zeller, in Korea

The apple ermine moth, Yponomeuta malinellus Zeller (Lepidoptera: Yponomeutidae), is a tent caterpillar that feeds on Malus spp. in Korea. Populations of the moth in native areas appeared to be regulated by the assemblage of parasitoids. Phenological associations between host stages and parasitoids, susceptible stage(s) of the host for each parasitoid, and stage‐specific parasitism were studied. The egg larval parasitoid Ageniaspis fuscicollis (Dalman) had highest parasitism of first instar larvae (24%), with 14% parasitism of other larval stages. Dolichogenidea delecta (Haliday) was recovered from all larval instars with the highest parasitism rate of second instar larvae (20.1%), followed by 19.9% parasitism of mid‐larval hosts. Herpestomus brunicornis Gravenhorst was reared from second instar larvae through to pupal collection, and had the highest parasitism rate (29.9%) at the pupal stage. The larval pupal parasitoid Zenillia dolosa (Meigen) was recovered from mid‐larval to pupal stages with the highest parasitism rate (5.5%) occurring in third to fourth instar larvae. The host stages for developing A. fuscicollis completely overlap with those of D. delecta, and with those of H. brunicornis to some degree. A statistically significant negative correlation exists between A. fuscicollis and these dominant parasitoids, indicating competitive interaction within the host.     

Egg Parasitoid Complex of the Corn Leafhopper, <Emphasis Type="Italic">Dalbulus maidis</Emphasis> (DeLong) (Hemiptera: Cicadellidae), in Argentina

The corn leafhopper, Dalbulus maidis (DeLong), is the most important leafhopper pest of maize, Zea mays, in the Americas. A survey of the diversity of its egg parasitoids was carried out in northwestern Argentina. During summer from 2004 to 2007, the samples were collected, using sentinel eggs of D. maidis on corn leaves, exposed in 48 cornfields. Sixteen species belonging to four families of Chalcidoidea (Hymenoptera) were identified. Among the parasitoid groups, Trichogrammatidae was the most represented family with eight species, followed by Mymaridae with six species. The mymarid Anagrus incarnatus Haliday and the trichogrammatid Pseudoligosita longifrangiata (Viggiani) were the most abundant and frequent parasitoids. The mean percentage of parasitism of D. maidis eggs was 16.4% and varied greatly among the sites, ranging from 0 to 56.7%; generally, it was higher in Yungas and lower in Monte province sites. The species richness was higher in the localities within the Yungas, with 13 parasitoid species, of which two species were dominant, comprising 83.6% of the collected individuals. Monte was the province that showed the highest diversity index (H´ = 1.62). In addition, we present information on the distribution, known host associations of each parasitoid species and an identification key to all species of egg parasitoids of D. maidis in Argentina.     

A molecular phylogeny of the tribe Aphidini (Insecta: Hemiptera: Aphididae) based on the mitochondrial tRNA/COII, 12S/16S and the nuclear EF1α genes

Abstract A phylogeny of the tribe Aphidini (Hemiptera: Aphididae) was reconstructed from three gene fragments: two mitochondrial regions, partial tRNA‐leucine + cytochrome oxidase II (tRNA/COII), partial 12S rRNA + tRNA‐valine + 16S rRNA (12S/16S) and one nuclear gene, the elongation factor‐1 alpha (EF1α). Bayesian phylogenetic (BP) analyses were performed on each individual dataset of tRNA/COII, 12S/16S and EF1α, and maximum parsimony (MP), Bremer support test, maximum likelihood (ML) and BP analysis were performed on the combined dataset. After comparing our molecular phylogenetic results with the classic classification based on morphological and ecological data, we analysed three main issues: the monophyletic relationships among tribes and subtribes, the validities of the latest taxonomic positions of genera and species and the status of certain Aphis species groups. Our results indicate that 36 of the species analysed, with the exception of Cryptosiphum artemisiae, are clustered within the clade of Aphidini. Also, the 28 species representative of the subtribe Aphidina were separated from the eight species representative of Rhopalosiphina; each monophyletic subtribe was supported by significant P‐values in the combined analysis. According to our results, Cryptosiphum should be moved to Macrosiphini because it is more closely related to the genera Lipaphis and Brevicoryne. The genus Toxoptera was recovered as non‐monophyletic. In Rhopalosiphina, three genera, Hyalopterus, Rhopalosiphum and Schizaphis, were relatively closer to each other than to the genus Melanaphis. In the relationships between species‐groups among Aphis, most species were separated into two main lineages; the fabae group seemed to be more closely related to the spiraecola and craccivora group rather than to the gossypii group.     

Phylogenetic patterns of mimicry strategies in Darnini (Hemiptera: Membracidae)

A phylogenetic analysis based on 58 morphological characters including 18 species representing 14 genera over the 15 currently known in Darnini (Hemiptera: Membracidae) confirms the monophyly of this tribe. This result is particularly supported by the presence of cucullate setae on the ventral side of the femora. Two sister clades are inferred: the clade Funkhouseriana+ which groups four genera (Aspona, Cyphotes, Funkhouseriana, Taunaya) and exhibits a ‘bird dropping’ habitus and all other genera which exhibit a ‘dewdrop’ like habitus (Alobia, Darnis, Dectonura, Hebetica, Hebeticoides, Leptosticta, Ochrolomia, Stictopelta) or a ‘thorny’ habitus (Alcmeone, Sundarion). In the ‘dewdrop’ habitus, only the clade Ochrolomia+ is retained as a monophyletic unit. According to these results, pronotal shapes and habitus have evolved independently in each monophyletic unit and each one seems correlated with a particular type of mimicry strategy. According to the strategy, characters involved are different, a priori independent; moreover, they look coordinated regarding to the mimicry function they serve. The various evolutionary scenarios are discussed in relation to the phylogeny, and particularly in correlation with the non-gregarious behavior of these membracids, also coherent with their mimicry strategy.     

Phylogenetic Placement of Pentatomid Stink Bug Gut Symbionts

Insect bacterial symbionts are ubiquitous, however, only a few groups of host families have been well studied in relation to their associations with microbes. The determination of the phylogenetic relationships among bacteria associated with different species within an insect family can provide insights into the biology and evolution of these interactions. We studied the phylogenetic placement of vertically transmitted bacterial symbionts associated with the posterior midgut (crypt-bearing) region of pentatomid stink bugs (Hemiptera, Pentatomidae). Our results demonstrate that different host species carried one major bacterium in their midgut. Phylogenetic analyses of the 16S rRNA gene sequences obtained from the midgut of stink bugs placed all symbionts in a clade with Erwinia and Pantoea species, both plant-associated bacteria. Results indicate that symbiont monophyly occurs among recently diverged taxa (e.g., within a genus) but does not occur in the Pentatomidae. Results suggest that these vertically transmitted symbionts are occasionally replaced by other taxonomically similar bacteria over evolutionary time. Our findings highlight how the evolutionary history of hemipteran symbionts in unexplored host families may have unpredictable levels of complexity.     

Two new records of Telenominae (Hymenoptera, Scelionidae) from the Rovno amber (Eocene of Ukraine)

Two new scelionid species of the subgenus Telenomus, genus Telenomus, subfamily Telenominae are described: Telenomus (Telenomus) oculus sp. nov. and T. (T.) tetragonus sp. nov. Brief morphological characterizations of the new taxa are given, and comparative analysis of the inclusions described and members of the recent fauna is provided.     

Identification of egg parasitoids of rice leafhoppers and planthoppers (Hemiptera: Cicadellidae and Delphacidae) of economic importance in Taiwan,part 1: Mymaridae (Hymenoptera)

Fairyfly egg parasitoids (Hymenoptera: Mymaridae) of rice leafhoppers and planthoppers (Hemiptera: Cicadellidae and Delphacidae) known from Taiwan are identified taxonomically, keyed, and illustrated. Their host associations are determined by rearings using sentinel eggs of mainly four key pest species. The previously published records of such egg parasitoids in Taiwan are critically analyzed in the unfortunate absence of almost any voucher specimens. Three species of Mymaridae are shown to be the predominant egg parasitoids of one leafhopper and three planthopper major pests of rice in Taiwan: Anagrus (Anagrus) incarnatus Haliday of the green rice leafhopper Nephotettix cincticeps (Uhler) and the delphacids Laodelphax striatella (Fallén) (small brown planthopper), Nilaparvata lugens (Stål) (brown planthopper), and Sogatella furcifera (Horváth) (whitebacked planthopper), as well as Gonatocerus aegyptiacus Soyka and Mymar taprobanicum Ward of N. cincticeps. The zig-zag leafhopper Maiestas dorsalis (Motschulsky), which is also common in paddy fields, is newly recorded as a host for A. incarnatus, G. aegyptiacus, Lymaenon litoralis (Haliday), and M. taprobanicum. Additional new records of some other Mymaridae in Taiwan, mostly from the rice field agroecosystems, are indicated. Litus assamensis Rehmat and Anis, syn. nov. from India, is synonymized with L. sutil Triapitsyn and Berezovskiy from Thailand, which is also newly recorded from Taiwan.     

Is It Possible to Manipulate Scelionidae Wasps’ Preference to a Target Host?

Parasitoid host selection is mainly mediated by chemical cues, which can be adjusted by experience, changing their innate behavior. Therefore, this study evaluated if immature experience (pre-imaginal conditioning) on eggs and volatiles from different host eggs has influence on parasitism and chemotaxic behavior of Telenomus podisi Ashmead and/or Trissolcus basalis Wollaston (Hymenoptera: Scelionidae). Both wasp species were submitted to a multiple-choice parasitism test among Euschistus heros (Fabricius), Piezodorus guildinii (Westwood), and Nezara viridula L. (Hemiptera: Pentatomidae) (Hemiptera: Pentatomidae) egg masses. Eggs from these three stink bugs were equally offered to female parasitoids. After that, adults which emerged from each host were also exposed to parasitism in a multiple-choice test for up to an additional generation. Moreover, in olfactometer “Y,” the behavior of innate and experienced T. podisi females to volatiles from hosts’ egg extracts was tested, to study their learning and memory ability. The original host had influence on T. podisi parasitism; however, T. basalis always parasitized more N. viridula eggs independently of its last rearing host. Innate T. podisi females responded positively to E. heros and P. guildinii egg volatiles, but this behavior was not observed in N. viridula. When T. podisi females were experienced on egg volatiles from a new host, they showed significant learning and memory ability for the specific host volatile for, at least, 24 h. Experienced wasps responded positively to N. viridula and through this result we have evidences about the possibility to manipulate wasp’s preferences to a specific target host.     

Interspecific larval competition between two egg parasitoids in refrigerated host eggs of Riptortus pedestris (Hemiptera: Alydidae)

In a previous study, we found that soybean fields could be supplemented with refrigerated eggs of Riptortus pedestris (Fabricius) (Hemiptera: Alydidae) to enhance parasitism. As a part of a study to evaluate the effect of host egg refrigeration on parasitism, host acceptance behavior and interspecific larval competition between Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae) and Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) were studied in multiparasitized unrefrigerated and refrigerated eggs. O. nezarae showed complete host acceptance behavior when offered refrigerated host eggs that were preparasitized by G. japonicum. Adult emergence rate of O. nezarae was 43 and 74% when the interval between the first and second oviposition was 0 and 4 days, respectively, and was not different between refrigerated and unrefrigerated eggs. Refrigeration did not change host acceptance behavior of G. japonicum, but adult emergence declined from 80% in unrefrigerated eggs to 37% in refrigerated eggs that were pre-parasitized by O. nezarae on the same day. No negative effects of refrigeration on sex ratio, adult longevity, and adult size of the both parasitoids were found. Generally host egg refrigeration did not negatively affect host acceptance behavior of the both parasitoids on preparasitized eggs or larval competition between the two parasitoids in multiparasitized host eggs with exceptions in the development time and emergence rate of G. japonicum. Therefore, host egg refrigeration may not interrupt interactions between the parasitoid populations in the field.     

Systematics and evolution of gall formation in the plant‐associated genera of the wasp subfamily Doryctinae (Hymenoptera: Braconidae)

Gall formation is a specialised form of phytophagy that consists of abnormal growth of host plant tissue induced by other organisms, principally insects and mites. In the mainly parasitoid wasp subfamily Doryctinae, gall association, represented by gall inducers, inquilines and their parasitoids, is known for species of seven genera. Previous molecular studies recovered few species of six of these genera as monophyletic despite their disparate morphologies. Here, we reconstructed the evolutionary relationships among 47 species belonging to six gall‐associated doryctine genera based on two mitochondrial and two nuclear gene markers. Most of the Bayesian analyses, performed with different levels of incomplete taxa and characters, supported the monophyly of gall‐associated doryctines, with Heterospilus (Heterospilini) as sister group. Percnobracon Kieffer and Jörgensen and Monitoriella Hedqvist were consistently recovered as monophyletic, and the validity of the monotypic Mononeuron was confirmed with respect to Allorhogas Gahan. A nonmonophyletic Allorhogas was recovered, although without significant support. The relationships obtained and the gathered morphological and biological information led us to erect three new genera originally assigned to Psenobolus: Ficobolus gen.n. (F. paniaguai sp.n. and F. jaliscoi sp.n. ), Plesiopsenobolus gen.n. (Pl. mesoamericanus sp.n. , Pl. plesiomorphus van Achterberg and Marsh comb.n. , and Pl. tico sp.n. ), and Sabinita gen.n. (S. mexicana sp.n. ). The origin of the gall‐associated doryctine clade was estimated to have occurred during the middle Miocene to early Oligocene, 16.33–30.55 Ma. Our results support the origin of true gall induction in the Doryctinae from parasitoidism of other gall‐forming insects. Moreover, adaptations to attack different gall‐forming taxa on various unrelated plant families probably triggered species diversification in the main Allorhogas clade and may also have promoted the independent origin of gall formation on at least three plant groups. Species diversification in the remaining doryctine taxa was probably a result of host shifts within a particular plant taxon and shifts to different plant organs. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:0021F253‐4ABA‐4EAA‐A7A9‐FC0AD1932EA3     

Effect of host switching on performance of mass‐reared Trichogramma minutum

The effect of host switching on parasitism by Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae) (TM) was examined for parasitoids attacking a factitious host, the Mediterranean flour moth, Ephestia kuehniella Zell. (Lepidoptera: Pyralidae) (MFM), and a natural host, the eastern spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae) (SBW). Parasitoids that were switched from rearing on the natural host to rearing on the factitious host had lower realized fecundities on both MFM and SBW eggs than a control line that was maintained continuously on the natural rearing host, SBW eggs. Conversely, T. minutum reared on the factitious host and switched to rearing on the natural host showed greater realized fecundities. This increase in realized fecundity was lost in the first generation after switching parasitoids back to the factitious rearing host. T. minutum that were maintained on the natural rearing host (SBW eggs) showed more variation in realized fecundity and host acceptance of both MFM and SBW eggs, than parasitoids that were reared on MFM eggs.     

Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study

In order to reduce parasite‐induced mortality, hosts may be involved in mutualistic interactions in which the partner contributes to resistance against the parasite. The pea aphid, Acyrthosiphon pisum Harris (Hemiptera: Aphididae), harbours secondary bacterial endosymbionts, some of which have been reported to confer resistance against aphid parasitoids. Although this resistance often results in death of the developing parasitoid larvae, some parasitoid individuals succeed in developing into adults. Whether these individuals suffer from fitness reduction compared to parasitoids developing in pea aphid clones without symbionts has not been tested so far. Using 30 pea aphid clones that differed in their endosymbiont complement, we studied the effects of these endosymbionts on aphid resistance against the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae: Aphidiinae), host–parasitoid physiological interactions, and fitness of emerging adult parasitoids. The number of symbiont species in an aphid clone was positively correlated with a number of resistance measurements but there were also clear symbiont‐specific effects on the host–parasitoid interaction. As in previous studies, pea aphid clones infected with Hamiltonella defensa Moran et al. showed resistance against the parasitoid. In addition, pea aphid clones infected with Regiella insecticola Moran et al. and co‐infections of H. defensa–Spiroplasma, R. insecticola–Spiroplasma, and R. insecticola–H. defensa showed reduced levels of parasitism and mummification. Parasitoids emerging from symbiont‐infected aphid clones often had a longer developmental time and reduced mass. The number of teratocytes was generally lower when parasitoids oviposited in aphid clones with a symbiont complement. Interestingly, unparasitized aphids infected with Serratia symbiotica Moran et al. and R. insecticola had a higher fecundity than unparasitized aphids of uninfected pea aphid clones. We conclude that in addition to conferring resistance, pea aphid symbionts also negatively affect parasitoids that successfully hatch from aphid mummies. Because of the link between aphid resistance and the number of teratocytes, the mechanism underlying resistance by symbiont infection may involve interference with teratocyte development.