The impact of kleptoparasitic invasions on the evolution of gall-size in social and solitary Australian Acacia thrips

Many species of gall-inducing Acacia thrips are attacked by kleptoparasitic thrips who enter the gall, destroy the occupants, and then use the gall for producing their own offspring. The hypothesis tested here is that pressure exerted by ldeptoparasites （genus Koptothrips） not only provoked the evolution of soldiers in the gall-inducing clade, but have also influenced the evolution of gall size and morphology. Various size dimensions of invaded galls were compared to those of uninvaded galls using data from six gall-inducing species and their kleptoparasites. For the non-social gall-inducing species （K. ellobus and K. nicholsoni） invaded galls showed no significant size differences from galls that had not been invaded. For the four social gall-inducingspecies （K. habrus, K. intermedius, K. waterhousei and K. morrisi） invaded galls were significantly narrower and/or shorter than uninvaded galls. Galls of social species that had not been invaded and contained adult soldiers were significantly larger than galls where soldiers were still at a larval stage, suggesting that gall size is related to gall age in these species. An hypothesis is proposed that links the timing of invasion by kleptoparasites to size of the host gall： induction of a smaller gall by host founders will reduce the period of vulnerability to invasion （before soldiers become adults） for social thrips by allowing foundresses in these smaller galls to begin laying soldierdestined eggs relatively sooner.     

Buying time for colony mates: the anti-predatory function of soldiers in the eusocial aphid Ceratovacuna japonica (Homoptera, Hormaphidinae)

Eusocial aphids produce sterile individuals (soldiers) that specialize in colony protection. Killing predators is often considered the main function of soldiers. In this study, we tested the effect of harassment by soldiers of a eusocial aphid, Ceratovacuna japonica (Homoptera, Hormaphidinae), on predation by this species’ natural enemy, the larvae of Atkinsonia ignipicta (Lepidoptera, Stathmopodidae). We experimentally introduced some aphids and a predator to petri dishes and compared the survivorship of first-instar reproductives in the presence and absence of soldiers. We showed that soldiers can reduce the rate of predation on their colony mates without killing the predators. When predators encountered soldiers, they did not attempt to prey on them. Instead, they evaded them and often started to make a nest by spinning silken threads. The soldiers, in contrast, waved their forelegs and attacked the predator, and they sometimes succeeded in grasping the predator’s body. Because the predator used its mandibles to remove any soldier that succeeded in grasping its body, the soldier did not kill the predator. The reduction of predation was apparently caused by the delay of predation resulting from the harassment behavior of the soldiers. In eusocial aphids, a defensive strategy that delays predation may buy the soldiers’ colony mates time to reproduce or to escape from the predator.     

Clonal mixing in the soldier-producing aphid Pemphigus spyrothecae (Hemiptera: Aphididae)

Illuminating the genetic relationships within soldier-producing aphid colonies is an essential element of any attempt to explain the evolution of the altruistic soldier caste. Pemphigus spyrothecae is a soldier-producing aphid that induces galls on the leaf petioles of its host (trees of the genus Populus). At least a quarter of the aphids within the clonally produced gall population are morphologically and behaviourally distinct first-instar soldiers that defend the gall population from predation. Using field trapping and microsatellites, we investigated the degree of clonal mixing within natural gall populations. Field trapping in the UK showed that all the migrants of P. spyrothecae and of two other Pemphigus species were wingless first-instar soldiers. The average degree of mixing estimated from trapping P. spyrothecae migrants was 0.68% (range = 0-15%). Microsatellite genotyping of 277 aphids from 13 galls collected in Italy revealed an average mixing level of 10.4% (range = 0-59%). Six galls contained more than one clone (range = 2-5 clones). Non-kin aphids were not restricted to the soldier caste but were evenly distributed across instars. An additional gall, from which 527 occupants were genotyped, contained 12 non-kin aphids distributed among nine clones, showing that clonal diversity can be high even when mixing is very low. These observations suggest that although soldiers migrate regularly and can moult and reproduce within foreign galls, clonal mixing in this species is generally low and is unlikely to provide a barrier to the evolution of investment by the aphid clones in an altruistic soldier caste.     

Soldiers with large weapons in predator-abundant midsummer: phenotypic plasticity in a eusocial aphid

Eusocial aphids produce sterile individuals (“soldiers”) that specialize behaviorally and morphologically to protect their colony from predators, while production of soldiers can negatively affect colony growth because of reproductive allocation and opportunity cost. Hence, a cost-saving soldier production strategy is expected to be favored. Here, we hypothesize that, to save the cost, a eusocial aphid Ceratovacuna japonica produces soldiers with smaller weapon in the season when predators are not abundant. The abundance of two specialist lepidopteran predators (i.e., Taraka hamada and Atkinsonia ignipicta) of C. japonica dramatically increased, and aphid colony size significantly decreased, from July to August. In line with these, the soldiers in August had larger weapons (i.e., frontal horns) than those in June, indicating a correlational increase in weapon size with predation pressure. We predict that a reliable prospective signal indicating the coming of midsummer (environmental temperature) induces mother aphids to produce soldiers with larger weapons. Experiments clarified that soldiers produced at 20 °C (typical temperature of July to August) had larger weapons than those produced at 15 °C (typical temperature of May to July). Such phenotypic plasticity appears to be adaptive to maximize the fitness of C. japonica under a temporally variable but predictable predation environment. These results indicate that C. japonica aphids not merely have distinctive reproductive—and soldier castes, but also produce differentially armed soldiers in a habitat with temporally changing predation risks.     

Maternal death relaxes developmental inhibition in nymphal aphid defenders

In certain aphids, first-instar nymphs defend their gall by attacking intruding arthropod predators. One correlate of such defensive behaviour is a lengthened duration of the first nymphal stadium during the galling phase of the life cycle. A prolonged first stadium allows a large army of first-instar defenders to accumulate, which may be advantageous for gall defence. The factors determining developmental delay have been unclear, however. Our field experiment with Pemphigus obesinymphae, a North American gall-forming aphid with defensive first-instar nymphs, tests whether first-stadium duration is influenced by the death of the colony''s fundatrix (mother). We killed fundatrices in certain galls, left those in control galls alive, and counted aphids in each stadium in each gall. Galls in which fundatrices were killed contained a lower proportion of first-instar defenders and more late-instar nymphs than did galls with living fundatrices, indicating that maternal death dramatically increased developmental rate of nymphs. Possibly nymphal aphids respond adaptively to environmental cues that signal a threat to the colony''s welfare. Alternatively, the fundatrix actively suppresses offspring development in order to maintain a large army of soldiers to protect her gall. The results add a new layer of complexity to our understanding of social aphid systems.     

Evidence for Caste Differences in Anal Droplet Alarm Pheromone Production and Responses in the Eusocial Thrips Kladothrips intermedius

Thrips (Thysanoptera) are tiny insects that produce anal secretions when threatened. Several studies have shown that, depending on the species, the droplets may contain alarm pheromones and/or repellents against enemies. In the eusocial gall‐inducing thrips Kladothrips intermedius both larvae and adults produce such droplets. There are two castes of adults in this species, soldiers (the sub‐fertile and gall‐bound defenders) and dispersers (winged and capable of initiating a gall). We tested the proclivity of secreting anal droplets by the two castes and whether the anal droplets induce different behavioural responses in relation to the emitter–receiver's caste in a contact chemoreception bioassay. Although secretion patterns were similar between castes, exposure to anal droplets emitted by different castes elicited different behavioural responses in adults in the bioassay. When exposed to soldiers’ anal droplets, dispersers significantly reduced the distance moved while soldiers significantly increased the distance moved, compared to when they were exposed to hexane control. In contrast, no differences in the distance moved were observed for any caste when exposed to dispersers’ anal droplets versus hexane control. Increased activity in soldiers when exposed to their own anal droplets is a predicted response to enhance the overall defence of the gall when under threat, whereas dispersers should slow down their activity when exposed to such ‘warning signal’. Thus, the behavioural data indicate that the anal droplets emitted by soldiers are likely to contain an alarm pheromone.     

An Endoparasitoid Avoids Hyperparasitism by Manipulating Immobile Host Herbivore to Modify Host Plant Morphology

Many parasitic organisms have an ability to manipulate their hosts to increase their own fitness. In parasitoids, behavioral changes of mobile hosts to avoid or protect against predation and hyperparasitism have been intensively studied, but host manipulation by parasitoids associated with endophytic or immobile hosts has seldom been investigated. We examined the interactions between a gall inducer Masakimyia pustulae (Diptera: Cecidomyiidae) and its parasitoids. This gall midge induces dimorphic leaf galls, thick and thin types, on Euonymus japonicus (Celastraceae). Platygaster sp. was the most common primary parasitoid of M. pustulae. In galls attacked by Platygaster sp., whole gall thickness as well as thicknesses of upper and lower gall wall was significantly larger than unparasitized galls, regardless of the gall types, in many localities. In addition, localities and tree individuals significantly affected the thickness of gall. Galls attacked by Platygaster sp. were seldom hyperparasitized in the two gall types. These results strongly suggest that Platygaster sp. manipulates the host plant''s development to avoid hyperparasitism by thickening galls.     

Does pre-dispersal seed predation limit reproduction and population growth in the alpine clonal plant Geum reptans?

We studied the impact of the seed damaging gall midge larva Geomyia alpina on its perennial alpine host plant Geum reptans. We analysed the effect of seed predation on reproduction by seeds, i.e. seed number, seed mass, and seed viability and on growth and clonal propagation of non-protected plants in comparison to plants protected from predation by an insecticide. Additionally, we assessed the consequences of seed predation for population growth using matrix projection modelling. Seed predation resulted in a decrease in total seed mass per flower head by 23.8% in non-protected plants (P < 0.05). Individual seed mass decreased with increasing infestation intensity (P < 0.05). Seed number remained unaffected because the sucking feeding behaviour by gall midge larvae does not evoke seed abortion. Percent germination of seeds from non-protected plants was reduced by 97.9% compared to seeds from protected plants. According to reduced seed viability, modelling revealed a decrease in population growth rate from λ = 1.055 to λ = 1.041. Predation did neither influence total plant biomass nor biomass fractions. But stolon dry-weight of non-protected plants increased by 24.1% (P < 0.05), which may indicate a trade-off between sexual reproduction and clonal propagation. Our results demonstrate that despite substantial reduction of viable seeds, predation by gall midge larvae only slightly affected population growth of G. reptans suggesting that in this alpine species, persistence by longevity and clonal propagation can balance potential seed losses by predation, at least for local population growth.     

Tuberaphis owadai (Homoptera), a new aphid species forming a large gall on Styrax tonkinensis in northern Vietnam

Tuberaphis owadai sp. nov., an aphid species forming coral‐shaped galls on Styrax tonkinensis in northern Vietnam, is described. We found that the species produces many sterile second‐instar soldiers in the gall. The colony size of a large gall was estimated to be 178 000, approximately half of which were soldiers. Alates emerging from galls contained sexual embryos, indicating that the life cycle is monoecious (non‐host‐alternating). Predaceous larvae of the pyralid moth Assara seminivalis were found in several galls.     

The effects of predation risk on the use of social foraging tactics

The effects of predation on the use of social foraging tactics, such as producing and scrounging, are poorly known in animals. On the one hand, recent theoretical models predict increased use of scrounging with increasing predation risk, when scroungers seeking feeding opportunities also have a higher chance of detecting predators. On the other hand, there may be no relation between tactic use and predation when antipredator vigilance is not compatible with scanning flockmates. We investigated experimentally the effects of predation risk on social foraging tactic use in tree sparrows, Passer montanus. We manipulated predation risk in the field by changing the distance between shelter and a feeder. Birds visited the feeder in smaller flocks, spent less time on it and were somewhat more vigilant far from shelter than close to it. Increased predation risk strongly affected the social foraging tactic used: birds used the scrounger tactic 30% more often far from cover than close to it. Between-flock variability in scrounging frequency was not related to the average vigilance level of the flock members, and within-flock variability in the use of scrounging was negatively related to the vigilance of birds. Our results suggest that in tree sparrows, the increased frequency of scrounging during high predation risk cannot simply be explained by an additional advantage of increasing antipredator vigilance. We propose alternative mechanisms (e.g. increased stochasticity in food supply, and that riskier places are used by individuals with lower reserves) that may explain increased scrounging when animals forage under high predation risk.     

Soldiers of a European gall aphid,Pemphigus spyrotecae (Homoptera: Aphidoidea): Why do they molt?

A non-migratory aphid,Pemphigus spyrothecae, produces 1 st-instar larvae of 2 types in the gall: thick-legged ones and normal-legged ones. It was found that the thick-legged larvae play a defensive role, hence they may be called soldiers. Unlike the soldiers of other species hitherto reported, at least some soldiers of this species molt and become adults. Their incomplete sterility is explained historically: 1) The migratory ancestor ofP. spyrothecae once produced monomorphic 1st-instar larvae attacking predators in the gall. 2) It acquired a non-migratory life cycle by the larviposition of emigrants in the gall. 3) As a result, 1 st-instar larvae of another morph, which had lived on the secondary host without attacking predators, joined the gall inhabitants. This hypothesis is supported strongly by the fact that the normal-legged 1 st-instar larvae very much resemble the 1 st-instar larvae of migratoryPemphigus species produced on the secondary hosts.     

Social biology and sex ratios of the eusocial gall-inducing thrips Kladothrips hamiltoni

1. Thrips comprise the only order besides Hymenoptera where females are diploid and males are haploid. This makes them useful insects for studying the roles of kin selection and ecology in social evolution. 2. Kladothrips hamiltoni is one of six species of Australian gall-inducing thrips that have been identified as eusocial. Galls are initiated by a single foundress, who rears her brood and remains within the enclosed gall for life. The adults of both sexes of her first brood cohort are morphologically distinct from the second generation, comprising a nondispersing soldier caste. The foundress and sib-mated soldiers jointly produce a second, dispersing generation, approximately 60–80% of which are produced by the soldiers. Mean per capita egg production of female soldiers is less than 33% that of the foundress. 3. Adult eclosion of soldiers is protandrous but the overall sex ratio of the soldiers lacks bias (52% male). Protandry of soldiers increases the probability that female soldiers will be inseminated soon after their eclosion and therefore lay fertilised, female eggs. The lack of bias could be due to a balance between local resource competition and local mate competition. Gender-specific defensive behaviour of soldiers with their enemies may also be important in explaining this unexpected sex ratio. 4. The dispersing generation has an overall extreme female bias (5.6% male). Soldier incest increases relatedness between females more than between males, such that the foundress is more related to her granddaughters than her daughters, and female soldiers are more related to their daughters than their sons (assuming within-gall relatedness < 1). A female bias in the offspring of soldiers should be preferred by both the foundress and soldiers as they are more related to soldier-produced dispersing females than any other thrips in the gall. Female bias in the dispersing generation will also reduce local mate competition between males. Both soldier incest and local mate competition may therefore contribute to the extreme female bias in the dispersing generation. 5. Selection pressures for sociality in gall-inducing thrips appear to be more similar to those in gall-inducing aphids and naked mole rats than to those in Hymenoptera.     

Head-plug defense in a gall aphid

The aphid Astegopteryx sp. forms a banana-bunch shaped gall consisting of several subgalls on Styrax benzoides in northern Thailand, and completes its life cycle on the tree, without migrating to secondary hostplants. We found that its soldiers had sclerotic, protruded heads with many spine-like setae, and that several soldiers cooperate to plug the ostiole of the subgall with these heads. Of 173 ostioles examined in the field, 90.8 % were plugged with no space among the guarding soldiers. Many eggs and sexuals were found within subgalls guarded by soldiers, and a number of males were found trying to intrude into these subgalls. However, they were blocked by guarding soldiers, and it was no easy task for them to intrude into subgalls. The same was true for some soldiers that had rushed out of the subgall. Guarding soldiers often prevented outside soldiers from coming back into the subgall. These findings suggest an interesting possibility that guarding soldiers might consequently select still active, reusable soldiers and strong males for sexual females in their subgall. Received 6 March 2005; revised 5 and 20 July 2005; accepted 27 July 2005.     

Variation in the Degree of Pectin Methylesterification during the Development of Baccharis dracunculifolia Kidney-Shaped Gall

Insect galls may be study models to test the distribution of pectins and arabinogalactan-proteins (AGPs) and their related functions during plant cell cycles. These molecules are herein histochemically and immunocitochemically investigated in the kidney-shaped gall induced by Baccharopelma dracunculifoliae (Psyllidae) on leaves of Baccharis dracunculifolia DC. (Asteraceae) on developmental basis. The homogalacturonans (HGAs) (labeled by JIM5) and the arabinans (labeled by LM6) were detected either in non-galled leaves or in young galls, and indicated stiffening of epidermal cell walls, which is an important step for cell redifferentiation. The labeling of HGAs by JIM7 changed from young to senescent stage, with an increase in the rigidity of cell walls, which is important for the acquaintance of the final gall shape and for the mechanical opening of the gall. The variation on the degree of HGAs during gall development indicated differential PMEs activity during gall development. The epitopes recognized by LM2 (AGP glycan) and LM5 (1–4-β-D-galactans) had poor alterations from non-galled leaves towards gall maturation and senescence. Moreover, the dynamics of pectin and AGPs on two comparable mature kidney-shaped galls on B. dracunculifolia and on B. reticularia revealed specific peculiarities. Our results indicate that similar gall morphotypes in cogeneric host species may present distinct cell responses in the subcelular level, and also corroborate the functions proposed in literature for HGAs.     

Mine and gall predation as top down regulation in the plant–insect systems from the Cretaceous of Negev, Israel

Fossil evidence of predation on leaf mines and galls opens the way to analyzing regulatory circuits in plant–insect interaction systems and assessing their evolutionary advancement. In the Cretaceous (mid-Turonian) flora of Negev, Israel, predation traces vary from the entire gall or mine excisions to minute punctures and slits over the mine tracks. Bite marks on the borders of predation holes representing different mouthpart morphologies may show how diverse the predators were. The efficiency of predation as a top down regulation force is attested on the basis of the gall and mine abundance, gall morphologies, mine configurations, co-occurrence of different mine types on leaves, and temporary mining. In turn, the regulation efficiency is considered as a criterion of evolutionary advancement of the plant–insect community as a whole. It is suggested that the coeval Cretaceous coastal and inland communities differed in the relative significance of top-down regulation.     

A test of geometric hypotheses for soldier investment patterns in the gall producing tropical aphidCerataphis fransseni (Homoptera,Hormaphididae)

Summary The gall-forming aphidCerataphis fransseni produces soldiers that defend against predators. Soldiers are produced soon after colony foundation and the number of soldiers increases nonlinearly during colony growth. The number of soldiers scales to the square-root of the number of non-soldiers and linearly to the surface area of the gall. This suggests that soldiers are produced to defend an area, for example the perimeter of the colony or the surface of the gall, rather than individual aphids.     

Seed predation,pathogen infection and life-history traits in Brassica rapa

Herbivory and disease can shape the evolution of plant populations, but their joint effects are rarely investigated. Families of plants of Brassica rapa (Brassicaceae) were grown from seeds collected in two naturalized populations in an experimental garden. We examined leaf infection by the fungus Alternaria, seed predation by a gall midge (Cecidomyiidae) and plant life-history traits. Plants from one population had heavier seeds, were more likely to flower, had less fungal infection, had more seed predation and were more fecund. Fungal infection score and seed predation rate increased with plant size, but large plants still had the greatest number of undamaged fruits. Spatial heterogeneity in the experimental garden was significant; seed predation rate and fecundity varied among blocks. An apparent tradeoff existed between susceptibility to disease and seed predation: plants with the highest fungal infection score had the lowest seed predation rate. Alternaria infection varied between populations, but the disease had no effect on fecundity. Seed predation did reduce fecundity. Damaged fruits had 31.4% fewer intact seeds. However, evidence for additive genetic variation in resistance to seed predation was weak. Therefore, neither disease nor seed predation was likely to be a strong agent of genetically based fecundity selection.     

Inbreeding ancestors: the role of sibmating in the social evolution of gall thrips

We used microsatellite data to estimate levels of inbreeding in four species of solitary gall thrips that are in the same clade as the six species with soldier castes. Three of the four species were highly inbred (Fis 0.54-0.68), and the other apparently mated randomly (Fis near zero). These estimates, combined with previous data from species with soldiers, suggest that inbreeding is a pervasive life-history feature of the gall-inducing thrips on Australian Acacia. Mapping of inbreeding estimates onto the phylogeny of the gall inducers showed that the ancestral lineage that gave rise to soldiers was apparently highly inbred, and therefore, inbreeding could have played a role in the origin of sociality within this group. Moreover, there was a trend from high levels of inbreeding at the origin of soldiers to low levels in the most derived species with soldiers, which exhibits the highest levels of reproductive division of labor and soldier altruism. These patterns are consistent with considerations from population genetics, which show that the likelihood of the origin of soldier altruism is higher in inbreeding populations but that, once soldiers have evolved, a reduction in inbreeding levels may facilitate the evolution of enhanced division of labor and reproductive skew.     

Gall size determines the structure of the Rabdophaga strobiloides host–parasitoid community

Abstract.  1. The relationship between gall size and mortality of the willow pinecone gall midge Rabdophaga strobiloides (Diptera: Cecidomyiidae) was examined by determining the fate of all galls in a 30-ha area in central Alberta, Canada over 4 years. It was found that gall size has a large effect on the type and intensity of mortality experienced by the gall midge, and consequently this factor has the potential to influence the dynamics of the host–parasitoid interaction through the creation of phenotypic refuges.
2. Total midge mortality ranged from 51% to 78% over the course of the study and was dominated by parasitism by Torymus cecidomyiae (Hymenoptera: Torymidae) and Gastrancistrus sp. (Hymenoptera: Pteromalidae) as well as predation by birds. Gall size had a strong, non-linear effect on the attack rates of each of these natural enemies.
3. Birds attacked the smallest size classes. Torymus cecidomyiae preferentially attacked medium diameter galls and thus avoided predation by birds in smaller galls. Gastrancistrus sp. preferentially attacked the largest galls and consequently suffered lower rates of predation by both T. cecidomyiae and birds.
4. This study emphasises the importance of understanding the interactions among mortality factors in order to describe adequately the susceptibility of R. strobiloides to parasitism and predation, and ultimately its population dynamics.