A phylogenetic analysis of higher-level gall wasp relationships (Hymenoptera: Cynipidae)

We present the most comprehensive analysis of higher-level relationships in gall wasps conducted thus far. The analysis was based on detailed study of the skeletal morphology of adults, resulting in 164 phylogenetically informative characters, complemented with a few biological characters. Thirty-seven cynipid species from thirty-one genera, including four genera of the apparently monophyletic Cynipini and almost all of the genera in the other tribes, were examined. The outgroup included exemplar species from three successively more distant cynipoid families: Figitidae (the sister group of the Cynipidae), Liopteridae and Ibaliidae. There was considerable homoplasy in the data, but many groupings in the shortest tree were nonetheless well supported, as indicated by bootstrap proportions and decay indices. Partitioning of the data suggested that the high level of homoplasy is characteristic of the Cynipidae and not the result of the amount of available phylogenetically conservative characters being exhausted. The analysis supported the monophyly of the Cynipini (oak gall wasps) which, together with the Rhoditini (the rose gall wasps), Eschatocerini and Pediaspidini formed a larger monophyletic group of gall inducers restricted to woody representatives of the eudicot subclass Rosidae. The inquilines (Synergini) were indicated to be monophyletic, whereas the Aylacini, primarily herb gall inducers, appeared as a paraphyletic assemblage of basal cynipid groups. The shortest tree suggests that the Cynipidae can be divided into three major lineages: one including the inquilines, the Aylacini genera associated with Rosaceae, and Liposthenes ; one consisting entirely of Aylacini genera, among them Aulacidea , Isocolus and Neaylax ; and one comprising the woody rosid gallers (the oak and rose gall wasps and allies), the Phanacis-Timaspis complex and the Aylacini genera associated with Papaveraceae.     

Alien herbivores and native parasitoids: rapid developments and structure of the parasitoid and inquiline complex in an invading gall wasp Andricus quercuscalicis (Hymenoptera: Cynipidae)

Abstract.

• 1 Rapid and substantial changes have occurred in the parasitoid and inquiline community associated with the agamic galls of Andricus quercuscalicis since it invaded Britain in the late 1950s. The number of parasitoid and inquiline species has risen from one to thirteen over a 15-year period. Although the number of species has been relatively consistent over the last 8 years, the species composition has changed considerably and in a highly characteristic way during this period.
• 2 The parasitoid complex can be divided into two broadly distinct sets of parasitoid species; one set attacks only the gall former whereas the other set concentrates on the inquilines living in the wall of the gall.
• 3 The most dramatic change, however, is in the abundance of inquilines which were reported to be virtually absent in earlier studies on this community in Britain. Over a period of only 5 years, between 1988 and 1993, inquiline attack rose from less than 0.01 to an average of 0.26 inquilines per gall. The intensity of inquiline attack is geographically heterogenous, with high inquiline numbers restricted to south-east England. Because of the relatively high specificity of the parasitoids, high inquiline abundance is positively correlated with parasitoid species richness in knopper galls.
• 4 Parasitism rates, particularly on the gall former, were generally low (<10%). Over the last 5 years, however, seven parasitoid species have been consistently recorded and the mortality caused by these species has increased continuously. The species composition of the community associated with this alien gall wasp in Britain has quickly converged to the community known from its native range in continental Europe. Parasitoid species known to attack the galls of A.quercuscalisis on the continent have been recorded from it in Britain for the first time mainly in areas where inquilines have recently become abundant.
• 5 Since rates of parasitism of the gall former are still low, parasitoids are unlikely to play a major role in the population dynamics of this invading gall wasp at present, but the rapidly increasing inquiline and parasitoid attack could be a source of increased mortality for native cynipid species which are the alternative hosts of those parasitoid species.

     

The effect of hosptlant and parasitoids on the reproductive success of the parthenogenetic gall wasp Diplolepis rosae (Hymenoptera,Cynipidae)

Summary The univoltine cynipid gall wasp Diplolepis rosae reproduces by an obligate homozygosity promoting system known as gamete duplication. The wasp is confined to roses (Rosa spp) on which it induces large, complex and multichambered galls. In southern Sweden, D. rosae was found to parasitize Rosa canina, R. dumalis, R. rubiginosa, R. villosa, R. sherardi and R. rubrifolia, but not R. majalis and R. rugosa. The distribution of galls shows that there are differences in the relation between wasp and hosplant with respect both to species and individual plants. There is a positive correlation between wasp size and gall (clutch) size. Parasitoid pressure was found to be high, causing D. rosae an estimated average larval loss of approximately 75%, mainly due to the attack of the ichneumonid wasp Orthopelma mediator. The very common cynipid inquiline Periclistus brandtii does not seem to have any negative effects. Overall parasitism and probability of no hatched offspring per gall decrease with increasing gall (clutch) size. The probability of loosing all of a given number of offspring decreases with the number of galls produced. It is suggested that D. rosae, in order to escape parasitoids, needs high ability to establish new colonies. Hence the production of many comparatively small galls, which increases the chance of leaving any offspring, rather than the production of few large galls, maximizing the number of offspring, should be favoured by selection.     

The advantage of attending ants and gall aggregation for the gall wasp Andricus symbioticus (Hymenoptera: Cynipidae)

Summary Gall clusters of Andricus symbioticus secrete a sweet and sticky food attractive to ants. An ant exclusion experiment demonstrated the selective advantage of attending ants and gall aggregation for A. symbioticus. This gall wasp interacts with the gall-attending ants only through the host plant. Evolution of this symbiotic relationship seems to be associated with gall aggregation.Contribution from Laboratory of Entomology Kyoto Prefectural University, No. 249     

The rearranged mitochondrial genome of Podagrion sp. (Hymenoptera: Torymidae), a parasitoid wasp of mantis

The complete sequence of the mitochondrial genome of Podagrion sp. (Hymenoptera: Torymidae) is described. The mitogenome was 15,845 bp in size, and contained typical sets of mitochondrial genes. The base composition of the Podagrion sp. mitogenome was also biased toward A + T bases (81.8%). The mitochondrial genome of Podagrion sp. has a weak AT skew (0.07) and a strong GC skew (?0.26). Podagrion sp. exhibits a novel rearrangement compared with the ancestral order, including six protein-coding genes (nad3, cox3, atp6, atp8, cox2 and cox1), which have inverted to the minor strand from the major strand. The A + T-rich region of Podagrion sp., which is located between trnN and trnI, have five tandem repeats. The apomorphic rearrangements, including the conserved block “cox3-atp6-atp8-cox2-cox1-nad5-nad4-nad4l-nad6-cob” and the special locations of trnV and trnA, were mapped onto the phylogeny of Proctotrupomorpha.     

Optimal clutch size of the chestnut gall-wasp,Dryocosmus kuriphilus yasumatsu (Hymenoptera: Cynipidae)

Optimal clutch size of the chestnut gall-wasp, Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), was examined in galls on wild and resistant chestnut trees in 1988 and 1989. The rate of escape success of newly-emerged adults from galls was an average of 60%, irrespective of cell numbers per gall. Dry mass per cell of a gall (as an index of nutritive condition) decreased with increasing cell number per gall, but was proportional to the mean number of mature eggs of new adults per gall. The number of cells per gall that occurred most frequently did not agree with that attained by the maximum survival rate from young larva to adult emergence of the gall-wasp. This discrepancy was examined from the viewpoint of three factors: 1) quality of offspring, 2) defensive response of the host plant causing mortality of the gall-wasp before cell formation, and 3) fitness per gall vs. fitness per egg. It is concluded that the third factor is most likely to be the one best in explaining the discrepancy.     

Single-locus sex determination in the parasitoid wasp Cotesia glomerata (Hymenoptera: Braconidae)

The parasitoid Cotesia glomerata usually produces female-biased sex ratios in the field, which are presumably caused by inbreeding and local mate competition (LMC); yet, sibling mating increases the production of males, leading to the male-biased sex ratio of broods in the laboratory. Previous studies have suggested that the sex allocation strategy of C. glomerata is based on both partial LMC in males and inbreeding avoidance in females. The current study investigated the presence of single-locus complementary sex determination (sl-CSD) as a sex-determining mechanism in this species through inbreeding experiment, cytological examination and microsatellite analysis. Cytological examination detected diploid males in nine of 17 single pairs of sibling mating, thus in agreement with the proportion of matched matings predicted by the sl-CSD model. Sex ratio shifts in these matched sibling matings were consistent with the sl-CSD model with less viable diploid males. The haploid males have a single set of maternal chromosomes (n = 10), whereas diploid males possess a double set of chromosomes (2n = 20). Microsatellite analyses confirmed that diploid males produced from the matched matings inherited segregating genetic materials from both parents. Thus, this study provides the first solid evidence for the presence of sl-CSD as a sex-determining mechanism in the braconid genus Cotesia.     

Efficiency and establishment of three introduced parasitoids of the mealybug Paracoccus marginatus (Hemiptera: Pseudococcidae)

Three introduced parasitoids Acerophagus papayae, Anagyrus loecki, and Pseudleptomastix mexicana of the mealybug Paracoccus marginatus have been released in Miami-Dade and Broward counties (Florida) in 2003. Efficiency and establishment of these previously introduced parasitoids to control P. marginatus were measured in 2005 and 2006, at three locations in Homestead (Miami-Dade). Mealybug populations were initially established on three branches (per plant) of 10 hibiscus plants inside closed-sleeve cages. The three treatments, closed, open, and no-cage environments were applied to the three established mealybug populations on each plant. The number of mealybugs and natural enemies was monitored in all treatments. After 72 h, the number of P. marginatus in the open-sleeve cage was higher than in the no-cage treatment but both were lower than the number in the closed-sleeve cage. Efficiency of parasitoids was evaluated by their percentage parasitism. Percentage parasitism (=recovery) was also used as an indicator for parasitoid establishment. Two of the three previously released parasitoids (A. papayae and A. loecki) were recovered in this study. Acerophagus papayae had a higher percentage parasitism than A. loecki in both the open-sleeve cage (31.0% vs 2.3%) and the no-cage treatments (21.4% vs 1.6%) and caused the most mortality of P. marginatus. There was no recovery of P. mexicana in either of the treatments. Although both A. papayae and A. loecki were established in tested areas, A. papayae was more efficient in controlling P. marginatus than A. loecki. The reasons for not recovering P. mexicana in release areas is yet unknown.     

Invaders on the move: parasitism in the sexual galls of four alien gall wasps in Britain (Hymenoptera: Cynipidae)

Four alien, host-alternating cynipid gall wasps are established in the British Isles: Andricus kollari, A. lignicola, A. quercuscalicis and A. corruptrix. Their current distributions divide Britain into four zones; all four invaders are present in the south and south-east of Britain, whereas only A. kollari is present in the far north of Scotland. The rank order, according to how far north the distributions of the four invading cynipid species reach, is: A. corruptrix→ A. quercuscalicis→ A. lignicola→ A. kollari. The life cycles of all four cynipid species involve a sexual generation in spring on Quercus cerris, and an agamic generation in autumn on Q. robur. Here we studied the parasitoid attack by four pteromalid species on the sexual generations of the invaders. We collected and reared the galls of all four species at eight sites from the south to the north of the country (two sites per zone). The geographical locations of the sites reflect the invasion history and thus the residence time of the alien species in the four zones. At each site we measured the densities of all host galls on Q. cerris and of both obligatory host-tree species. We also took a series of measures, such as host-tree density and mean host-tree size, to further characterize the tree stands. These measures are referred to as local parameters. Host densities varied between sites and between years. In A. kollari, galling rates were highest in the middle of the country (zone 2) in 1994, whereas in 1995 they increased from the south to the north. In A. lignicola, galling rates in both years were lowest at the sites in zone 3 (closest to its distribution boundary). In A. quercuscalicis, galling rates were found to be lowest at the site most to the north-west in both years, again the one furthest away from the area where this species was first recorded. Mortality caused by parasitoid attack differed from less than 10% to as high as 70% and varied between host species, sites and years. In four out of six cases the historical/regional variables (north/south and east/west) correlated significantly with parasitoid attack rates that were characteristically lowest at sites close to the distribution boundaries. Of the local factors, we found parasitoid attack rates correlated negatively in one case with host density, whereas they correlated positively in four cases with the density of alternative hosts of the parasitoids. In one of the models the local density of Q. cerris trees correlated negatively with parasitoid attack on A. quercuscalicis. For all three host species the terms retained in the minimal adequate models obtained for 1994 and 1995 differed, which might indicate that these communities of native parasitoids and invading host have not yet settled in any definite structure.     

Functional and nonfunctional female receptivity signals in the parasitoid wasp Spalangia endius (Hymenoptera: Pteromalidae)

In many taxa, females signal during courtship when they are receptive. However, just because a female signals does not mean that the male responds to the signal. This study examines female signaling of receptivity (readiness to copulate) and male response in the parasitoid wasp Spalangia endius Walker. Females folded their antennae against their heads when they were receptive, and antennal folding has been shown to be effective in eliciting male copulation attempts in a confamilial. However, male S. endius did not respond to antennal folding: males did not contact the female's antennae during courtship, and how quickly a male attempted copulation was independent of whether or not the female had antennae. Males courted from on top of the female's abdomen and appeared to detect receptivity directly from the female's abdomen rising as her genital orifice opened. On females whose abdomens did not rise, initiation of male copulation attempts were delayed but not eliminated. Based on its current lack of function as a receptivity signal and on comparisons to published reports of mating behavior in confamilials, we hypothesize that female antennal folding at receptivity is a vestigial trait in S. endius.     

Developmental rates of the aphid Aphis pomi (Aphidoidea: Aphididae) and its parasitoid Aphidius ervi (Hymenoptera: Aphidiidae)

Developmental rates of the aphid Aphis pomi and its parasitoid Aphidius ervi were compared at four constant temperatures (15, 20, 25, 30°C). Aphis pomi required 159.07 degree-days (DD) above lover developmental threshold (LDT) of 0.3°C. Aphidius ervi required 229.73 DD above LDT of 5.98°C. Developmental rate of A. pomi is higher than the developmental rate of A. ervi at the same conditions     

Host-plant mediated effects of transgenic maize on the insect parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae)

Determining the impact of genetically modified (GM) crops on beneficial organisms is an important aspect of the environmental risk assessment of GM crops. In the present study, the impact of Bt maize expressing Cry1Ab on the development and behaviour of the parasitoid Campoletis sonorensis was compared to individuals reared on hosts fed conventionally bred plants partially resistant to the European corn borer (Ostrinia nubilalis Hübner) and on susceptible maize hybrids. Adult parasitoids reared on Bt maize-fed Spodoptera frugiperda larvae were significantly smaller (15–30%) than those reared in hosts fed either of the conventional maize hybrids. The magnitude of this effect was dependent on the size of the host at oviposition and its subsequent growth rate. The development time of C. sonorensis was not affected by the maize treatment. In choice tests, female parasitoids displayed no preference for hosts fed a specific maize hybrid. No Cry1Ab was detected within adult parasitoids.     

Using the literature to evaluate parasitoid host ranges: a case study of Macrocentrus grandii (Hymenoptera: Braconidae) introduced into North America to control Ostrinia nubilalis (Lepidoptera: Crambidae)

We propose a method for using the literature to evaluate host ranges of parasitoids that are candidates for biological control introductions. Data on the parasitoids that attack a given host species can be used as negative evidence concerning the candidate whose host range is being evaluated. By compiling studies for a variety of host species, one can delineate those taxa unlikely to be attacked by the candidate. Using a retrospective case study of a parasitoid introduced into North America, we describe (1) this approach to using the literature to evaluate host range and (2) how well predictions based on such an evaluation match actual host range. Based on the host range of Macrocentrus grandii in Eurasia as reported in the literature, we predicted that the species in the genus Ostrinia are the most likely hosts. Of native North American species, Ostrinia obumbratalis is the only non-target species likely to be attacked by M. grandii. The predicted host range for North America matched the actual host range found in the field. This suggests that a careful literature review could be used as an important source of data on host range of parasitoid species proposed for introduction into a new environment.     

Incidence of the introduced parasitoids Cotesia kazak and Microplitis croceipes (Hymenoptera: Braconidae) from Helicoverpa armigera (Lepidoptera: Noctuidae) in tomatoes, sweet corn, and lucerne in New Zealand

Morphological defense traits of plants such as trichomes potentially compromise biological control in agroecosystems because they may hinder predation by natural enemies. To investigate whether plant trichomes hinder red imported fire ants, Solenopsis invicta Buren (Hymenoptera: Formicidae), as biological control agents in soybean, field and greenhouse experiments were conducted in which we manipulated fire ant density in plots of three soybean isolines varying in trichome density. Resulting treatment effects on the abundance of herbivores, other natural enemies, plant herbivory, and yield were assessed. Trichomes did not inhibit fire ants from foraging on plants in the field or in the greenhouse, and fire ant predation of herbivores in the field was actually greater on pubescent plants relative to glabrous plants. Consequently, fire ants more strongly reduced plant damage by herbivores on pubescent plants. This effect, however, did not translate into greater yield from pubescent plants at high fire ant densities. Intraguild predation by fire ants, in contrast, was weak, inconsistent, and did not vary with trichome density. Rather than hindering fire ant predation, therefore, soybean trichomes instead increased fire ant predation of herbivores resulting in enhanced tritrophic effects of fire ants on pubescent plants. This effect was likely the result of a functional response by fire ants to the greater abundance of caterpillar prey on pubescent plants. Given the ubiquity of lepidopteran herbivores and the functional response to prey shown by many generalist arthropod predators, a positive indirect effect of trichomes on predation by natural enemies might be more far more common than is currently appreciated.     

Geographic and between-generation variation in the parasitoid communities associated with an invading gallwasp,Andricus quercuscalicis (Hymenoptera: Cynipidae)

The knopper gallwasp Andricus quercuscalicis Burgsdorf 1783 (Hymenoptera: Cynipidae) has invaded western and northern Europe from southern and eastern Europe over the last 400 years. A. quercuscalicis has two alternating generations, which differ in phenology, structure, and host oak species. This study describes geographic variation in the community in the tiny catkin galls of the sexual generation on Turkey oak, Quercus cerris, and compares the patterns obtained with those in the community attacking the alternate agamic generation. As predicted from considerations of parasitoid recruitment to the communities of invading phytophagous insects (Cornell and Hawkins 1993), in its native range the sexual generation shows (1) higher parasitoid community species richness, (2) higher total mortality due to parasitoid attack and (3) a higher ratio of specialist to generalist parasitoid species than is evident in the invaded range. Counter to predictions, there is no indication that parasitoid community richness in the invaded range has increased with time since the arrival of the new host. Higher host mortality in the native range is due principally to a single specialist, Aulogymnus obscuripes Mayr 1877 (Hymenoptera: Eulophidae), and is not distributed evenly among parasitoid species which attack the gall-former only in this area. This contrasts with the community in Britain, where three principal generalist parasitoids cause approximately equal mortalities. The agamic gall contains a taxonomically and structurally diverse guild of parasitoid and inquiline species, associated with the changing resource provided by a large, long-lived, complex gall. In contrast, the sexual community includes a taxonomically and structurally narrow guild, associated with a resource which is structurally simple, small in size and short-lived. No parasitoid species attacks the gall-former in both generations. Surprisingly, in spite of these differences in the nature of the gall resource in the two generations, over their entire range (native and invaded) the parasitoid guilds of the two are equally species rich.     

Genetics of female functional virginity in the parthenogenesis-Wolbachia infected parasitoid wasp Telenomus nawai (Hymenoptera: Scelionidae)

A lepidopteran egg parasitoid species Telenomus nawai consists of two distinct populations with different reproductive modes. One is a completely thelytokous population consisting of females only, whereas the other displays arrhenotokous reproduction where fertilized eggs develop into diploid females and unfertilized eggs into haploid males. Thelytoky in T. nawai is caused by a bacterial symbiont, the parthenogenesis-inducing (PI) Wolbachia. Recent theoretical studies have shown that when a PI-Wolbachia is spreading in a population, mutations that allow uninfected females to produce more male offspring will spread rapidly eventually becoming fixed. The consequence of such a mutation is that sexual reproduction is no longer successful in infected females. Here we determine the genetic basis of the females' inability to reproduce sexually by introgressing the genome of a thelytokous line into an arrhenotokous line. The results suggest that the mutations are recessive and inherited either as a single-locus major gene with some modifiers, or as two partially linked loci.     

Isolation of novel microsatellite markers for the social parasitoid wasp, Copidosoma floridanum (Hymenoptera: Encyrtidae)

We developed and characterized nine microsatellite loci for the polyembryonic wasp Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae). Eight of the nine loci were polymorphic and did not deviate from Hardy–Weinberg equilibrium. Our results will contribute to studies on the population genetic structure of C. floridanum.     

Identification of 21 polymorphic microsatellites in the African parasitoid wasp, Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae)

We have developed 21 dinucleotide repeat microsatellite loci from African populations of Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae), a parasitoid wasp of the olive fruit fly, as part of a study assessing the role of introgression/hybridization in the success of a biological control introduction. We proposed suitable conditions for polymerase chain reaction multiplexing. All 21 loci were polymorphic with two to 21 alleles per locus within the Kenyan and South African populations tested. Most of them were successfully amplified in two other Psyttalia species.     

Effect of wasp size, physiological state, and prior host experience on host-searching behavior in a parasitoid wasp (Hymenoptera: Ichneumonidae)

Host-searching behavior in insects generally varies among individuals. A number of physiological and environmental factors can be involved in such individual variation. Here, a series of behavioral observations were made to highlight the importance of physiological state (i.e., number of mature eggs a female carries, amount of nutrient reserves, etc.) and learning state (i.e., prior host experience) on host-approaching behavior of parasitoids. Itoplectis naranyae (Hymenoptera: Ichneumonidae), a solitary endoparasitoid wasp attacking lepidopteran pupae and prepupae, was used as a test insect. The results show that female wasps with experience ovipositing on hosts 2 days before the test found hosts more quickly than did naïve wasps. Prior experience of host odor itself did not affect host-finding behavior, however. A single oviposition was enough for wasps to shorten time to find a host; additional experience had no significant effect on the efficiency of searching. The number of mature eggs a female carried had no effect on the time required to find a host regardless of prior host experience. The size of wasps, instead, was a significant factor when wasps had no prior host experience, and larger wasps found hosts more rapidly than did smaller wasps. Searching activity was not affected by how many hosts a female wasp had fed on before testing.     

The effect of superparasitism on development of the solitary parasitoid wasp, Venturia canescens (Hymenoptera: Ichneumonidae)

Abstract.

• 1 The effects of superparasitism on the rate of development, adult size and mortality of Venturia canescens (Hymenoptera: Ichneumonidae) were investigated. Parasitoids were reared from third (L3) and fifth (L5) instars of one of its hosts, Plodia interpunctella (Lepidoptera: Pyralidae) containing one, two or four parasitoid eggs.
• 2 Superparasitism increased the development time of Venturia reared from both instars, but the developmental delay was more evident in wasps from L5 hosts.
• 3 The size of parasitoids from L3 hosts was unaffected by egg number, but wasps from both superparasitized L5 treatments were significantly smaller than those from singly parasitized hosts.
• 4 Parasitoid mortality was significantly higher in L5 than L3, but within instars did not differ significantly with egg number.
• 5 The results confirm that superparasitism may affect the fitness of both the adult female wasp and her progeny, and should therefore be incorporated into models of superparasitism as an adaptive foraging strategy.