The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids

Abstract Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal trans-mission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts haveachieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont-conferredresistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show thatdefensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of thehost-parasitoid interaction, and by inducing environment-dependent trade-offs. These effects are conducive to very dynamic, symbiont-mediated coevolution that is driven by frequency-dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem byexploiting the parasitoids＇ demonstrated ability to rapidly evolve counteradaptations to symbiont-conferred resistance.     

Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts

Insects harbour a wild diversity of symbionts that can spread and persist within populations by providing benefits to their host. The pea aphid Acyrthosiphon pisum maintains a facultative symbiosis with the bacterium Hamiltonella defensa, which provides enhanced resistance against the aphid parasitoid Aphidius ervi. Although the mechanisms associated with this symbiotic‐mediated protection have been investigated thoroughly, little is known about its evolutionary effects on parasitoid populations. We used an experimental evolution procedure in which parasitoids were exposed either to highly resistant aphids harbouring the symbiont or to low innate resistant hosts free of H. defensa. Parasitoids exposed to H. defensa gained virulence over time, reaching the same parasitism rate as those exposed to low aphid innate resistance only. A fitness reduction was associated with this adaptation as the size of parasitoids exposed to H. defensa decreased through generations. This study highlighted the considerable role of symbionts in host–parasite co‐evolutionary dynamics.     

Genotype specificity among hosts,pathogens, and beneficial microbes influences the strength of symbiont‐mediated protection

The microbial symbionts of eukaryotes influence disease resistance in many host‐parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host‐parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host‐symbiont and symbiont‐pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co‐occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host's parasites.     

A defensive endosymbiont fails to protect aphids against the parasitoid community present in the field

1. The value of protective mutualisms provided by some facultative endosymbionts has been well demonstrated in the laboratory, yet only recently has their effectiveness in the field been studied. ‘Candidatus Hamiltonella defensa’ is known to defend aphids from parasitoid wasps in laboratory trials. However, the efficacy of this defence varies among parasitoids, suggesting that protection will vary spatially and temporally depending on parasitoid community composition. 2. This demonstrated specificity and a dearth of studies on Hamiltonella in the field prompted the authors to quantify parasitism rates of Hamiltonella‐infected and ‐uninfected Aphis craccivora Koch aphid colonies in a manipulative field study. 3. It was found that A. craccivora in central Kentucky alfalfa were parasitised by Lysiphlebus testaceipes (Cresson) and Aphelinus sp. Surprisingly, Hamiltonella infection did not lower successful parasitism by the naturally occurring parasitoid wasps. Whether Hamiltonella was effective against L. testaceipes was subsequently tested in a controlled laboratory assay, and no effect on parasitism rate was found. 4. This study emphasises the fact that defensive symbionts sometimes provide no tangible defensive benefits under field conditions, depending on parasitoid community composition. It is hypothesised that the protective mutualism may be beneficial in geographically localised areas. When the symbiosis is effective against a local parasitoid community, aphid clones may experience eruptive population growth and rapidly disperse across a large area, allowing spread to habitats with different parasitoid communities where the mutualism is an ineffective defence.     

Responses to aphid sex pheromones by the pea aphid parasitoids Aphidius ervi and Aphidius eadyi

Aphidius ervi and Aphidius eadyi, two parasitoids of the pea aphid Acyrthosiphon pisum, were attracted to components of the aphid sex pheromone in laboratory bioassays. Pre-test experience with host aphids in the presence of aphid sex pheromone did not affect the response of A. ervi to pheromone in a 4-way olfactometer, compared with that of naive parasitoids. Aphidius ervi females exposed only to the pheromone prior to testing did not respond in the olfactometer, suggesting habituation to the foraging cue by the parasitoid. In a wind tunnel, aphid sex pheromone increased the attraction of A. ervi to the plant-host complex (Vicia faba/A. pisum), suggesting an additive effect when two different foraging cues are present simultaneously.     

Spatial patterns and sampling plans for cereal aphids [Hom.: Aphididae] killed by entomophthoralean fungi and hymenopterous parasitoids in spring wheat

Cereal aphids infesting spring wheat in southwestern Idaho were surveyed during 1988 and 1989 for the presence of entomophthoralean fungi and hymenopterous parasitoids. Cereal aphids killed by the fungi (cadavers) and parasitoids (mummies) includedDiuraphis noxia (Mordvilko),Metopolophium dirhodum (Walker),Sitobion avenae (F.), andSchizaphis graminum (Rondani). Taylor's power law was used to describe the relationships between mean densities of cadavers or mummies (number per tiller) and associated variances. Except forS. graminum mummies, which were at low levels throughout the growing seasons and tended to be randomly distributed, Taylor's slopes exceeded 1.0 for all the aphid cadavers and mummies, indicating varying degrees of clumping in spatial pattern. The spatial patterns ofD. noxia andM. dirhodum cadavers were similar, simply reflecting those of their own populations, but more aggregated than were their respective mummies resulting from parasitoid attack. The intercepts and slopes from the power law analysis were used to generate functional relationships between the proportion of wheat tillers bearing cadavers or mummies of each aphid species and the mean density, and develop optimal numerical (direct counting) and binomial (presence or absence) sample size curves for both cadavers and mummies of each aphid species.      

The reactions of two cereal aphid parasitoids, Aphidius uzbekistanicus and A. ervi to host aphids and their food-plants

ABSTRACT. A Y-tube olfactometer was used to test the reactions of the hymenopteran cereal aphid parasitoids Aphidius uzbekistanicus Luzhetski and A. ervi Haliday to odours from aphids and their host plants. Only females responded to aphids but both sexes responded to plant odours. A. uzbekistanicus responded to the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Walker) whilst A. ervi , which has a broad host range, responded to M. dirhodum and the pea aphid, Acyrthosiphon pisum. Female A. uzbekistanicus responded to wheat leaves only but males responded to a range of plant material. Both male and female A. ervi responded to wheat and bean leaves. The failure of A. ervi to respond to either nettle aphids, Microlophium carnosum (Bukt.), or nettle leaves, despite its frequent parasitization of this aphid in the field, suggests the existence of more than one race of the parasitoid and casts doubts on the usefulness of alternative hosts as reservoirs for A. ervi in integrated control programmes. Males of both species responded to their respective females suggesting the presence of a sex specific attractant.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Increased reproduction by pea aphids in the presence of secondary parasitoids

1. The influence of the presence of secondary parasitoids on aphid reproduction was tested in a field experiment. 2. Single pea aphids Acyrthosiphon pisum in clip cages on potted bean plants were exposed to a collection of secondary parasitoids enclosed within a small perforated bag. The aphids were exposed to volatile chemicals released by the secondary parasitoids but there was no physical contact. 3. The production of nymphs was recorded over an 11‐day period. Aphids produced significantly more offspring in the presence of secondary parasitoids than in the absence of secondary parasitoids (36.9 vs. 31.2). 4. This is the second reported occurrence of this phenomenon, and the reasons for its occurrence and its consequences for aphid population and community ecology are discussed.     

Biology and trophic interactions of lucerne aphids

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Honeydew as a contact kairomone for aphid parasitoids

Aphidius rhopalosiphi De Stefani-Perez, four other primary parasitoids and three hyperparasitoids of cereal aphids responded to cereal aphid honeydew on filter paper discs by greatly increasing visit times. Both female and male parasitoids responded, females generally more strongly. A. rhopalosiphi females were shown to habituate to honeydew, and to dishabituate fully in 90 min. Their response increased with increasing concentrations of honeydew up to 0.25 mg/l, but no further increase was detected at 0.5 mg/l. The response did not occur when direct contact with the treated paper was prevented. A. rhopalosiphi responded to some honeydew from non-host aphids as strongly as to that from host aphids. A. rhopalosiphi responded to the honeydew produced by Metopolophium dirhodum (Walker) reared on artificial diet and to the diet itself as strongly as to honeydew from M. dirhodum reared on wheat. The response of A. rhopalosiphi to honeydew therefore appears not to be caused by specific plant chemicals in the honeydew, and is probably not caused by aphid-specific chemicals. The results are discussed in relation to host location by A. rhopalosiphi.

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Résumé Les parasitoïdes primaires de pucerons des céréales: Aphidius rhopalosiphi, A. picipes, A. ervi, Praon volucre et Ephedrus plagiator, ainsi que leurs hyperparasitoïdes, Dendrocerus carpenteri, Phaenoglyphis villosa et Alloxysta victrix ont réagi à du miellat de Sitobion avenae imbibant des disques de papier filtre, en prolongeant beaucoup leur temps de visite. Les femelles et les mâles ont réagi, mais les femelles généralement plus fortement. L'augmentation du temps de visite était probablement provoqué par la diminution de leur vitesse dans les zones traitées, leur tendance à séjourner dans ces zones et à y retourner après les avoir quittées.Les femelles de A. rhopalosiphi s'habituaient au miellat, mais s'en déshabituaient totalement en 90 minutes. Leurs réactions augmentaient avec la concentration en miellat jusqu'à 0,25 mg/l, sans qu'il y ait eu une nouvelle augmentation à 0,5 mg/l. La réaction était supprimée en absence de contact direct avec le papier. A. rhopalosiphi a repondu à quelques miellats produits par des non-hôtes aussi fortement qu'à celui de ses hôtes. A. rhopalosiphi a réagi au miellat produit par Metopolophium dirhodum, élevé sur milieu artificiel, et au milieu nutritiflui-même, aussi fortement qu'au miellat de M. dirhodum élevé sur du blé. Ainsi, la réponse d'A. rhopalosiphi à un miellat apparait comme n'étant pas due à la présence de substances chimiques spécifiques de plantes, ni, probablement, à des substances produites par les pucerons. Les résultats sont discutés en relation avec la localisation de l'hôte par A. rhopalosiphi.

     

The responses ofPraon spp. parasitoids to aphid sex pheromone components in the field

In autumn 1991, aphid parasitoids of the genusPraon (Hymenoptera; Braconidae) were caught in water traps with lures containing synthetic aphid sex pheromone components at three sites in England and one in Germany. At two of the English sites and at the German site, the traps were placed in winter cereal fields whilst the third English site was in woodland. Three species were caught,P. volucre, P. dorsale andP. abjectum. Those caught in cereal fields were almost entirelyP. volucre, whilstP. dorsale dominated at the woodland site. Of the known aphid sex pheromone components, the most effective lure was the (+)-(4aS, 7S, 7aR)-nepetalactone. Nepetalactone traps placed at the woodland site in spring and summer caught fewPraon females, and attraction may be confined to the autumn, when sexual female aphids are present in the field. Male parasitoids did not respond to the aphid pheromones at any time, although they were caught in suction traps operated at the woodland site during the autumn. At the cereal sites height had a significant influence on the efficiency of the pheromone traps, those placed just above the crop canopy being most effective. There was no evidence that any other genus of parasitoid responded to aphid sex pheromones at these sites.     

The evolutionary ecology of symbiont‐conferred resistance to parasitoids in aphids

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal transmission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont‐conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host–parasitoid interaction, and by inducing environment‐dependent trade‐offs. These effects are conducive to very dynamic, symbiont‐mediated coevolution that is driven by frequency‐dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem by exploiting the parasitoids’ demonstrated ability to rapidly evolve counteradaptations to symbiont‐conferred resistance.     

Individual behaviour and population dynamics: lessons from aphid parasitoids

An increasing number of researchers are studying behaviour in the hopes of understanding population dynamics or improving biological control efforts of insect pests by natural enemies. However, it is unclear exactly how behavioural studies will improve our understanding of these population level processes. In this paper we argue that in order to understand population level processes, the problem must be approached from a population biology perspective. A comprehensive understanding of certain behaviours will provide little towards our understanding of host-natural enemy interactions. For example, using an aphid-parasitoid model, we examined the effect that a commonly studied behaviour, variance in host selection by aphid parasitoids, has on aphid-parasitoid population dynamics. Differential host selection does not qualitatively alter classic Nicholson-Bailey dynamics, but only results in quantitative differences in aphid-parasitoid population sizes. Irrespective of the degree of aphid instar preference, a large increase in the number of aphids is followed by a large increase in the number of parasitoids, decimating the aphid population. Thus, studying some behaviours, such as variance in host selection, will not contribute substantially to an understanding of aphid-parasitoid population dynamics.     

The significance of a facultative bacterium to natural populations of the pea aphid Acyrthosiphon pisum

Abstract. 1.  Laboratory studies have implicated various accessory bacteria of aphids as important determinants of aphid performance, especially on certain plant species and under certain thermal regimes. One of these accessory bacteria is PABS (also known as T-type), which is distributed widely but is not universal in natural populations of the pea aphid Acyrthosiphon pisum in the U.K.
2.  To explore the impact of PABS on the performance of A. pisum , the nymphal development time and fecundity of aphids collected directly from natural populations and caged on the host plant Vicia faba in the field were quantified. Over 4 consecutive months June–September 1999, the performance of PABS-positive and PABS-negative aphids did not differ significantly.
3.  Deterministic modelling of the performance data showed that the variation in simulated population increase of PABS-positive and PABS-negative aphids would overlap substantially.
4.  Analysis of aphids colonising five host plants ( Lathyrus odoratus , Medicago sativa , Pisum sativum , Trifolium pratense , Vicia faba ) between April and September 2000 and 2001, identified no robust differences between the distribution of PABS-positive and PABS-negative aphids on different plants and with season or temperature.
5.  It is concluded that PABS is not an important factor shaping the performance or plant range of A. pisum under the field conditions tested. Reasons for the discrepancies between this study and laboratory-based studies are considered.     

纤毛类原生动物中宿主—共生体系统的研究

目前已经在100多种纤毛虫中观察到细菌、藻类和其他微生物等共生体。对纤毛虫中宿主－共生体系统的研究表明,双小核草履虫中卡巴粒的遗传为细胞质遗传理论提供了例证;含细菌共生体的许多厌氧纤毛虫无线粒体,共生体对宿主代谢有重要作用;尾草履虫－钝状全孢螺菌共生作用中,共生菌感染形式的39kDa、15kDa周质蛋白可分别与IF－3－1、IF－3－2两种单抗反应,其共生体早期感染过程中两种抗原的量发生显著变化,并且共生体生殖形式选择性地合成63kDa蛋白质,该蛋白质可能是与共生作有联系的关键分子;绿草履虫－小球藻共生系统中,共生藻中存在葡糖胺硬性壁是其与草履虫发生共生关系的基本条件,其中,共生藻参与宿主代谢,与宿主形成相互受益的专一性关系,并且藻类共生体的作用可能影响了宿主草履虫基因组有关结构,改变了其基因表达。作者推测,探索共生体对宿主基因结构及其表达产物的影响可能是对纤毛虫中共生作用研究的主要趋势,这对于深入了解真核细胞中宿主－共生体双方的相互作用、物质交流在分子水平上的调控机理、细胞结构与功能的关系等细胞生命活动规律是有意义的。     

Differential attraction of parasitoids in relation to specificity of kairomones from herbivores and their by-products

Infochemicals are used by foraging parasitoids in the host selection process from habitat preference until host recognition. Kairomones from the herbivore host plays a vital role in the attraction of parasitoids, particularly in the micro-habitat. Parasitoids are specifically attracted to their respective herbivore species even when different herbivores are present on the same plant. Chemicals emitted from different stages of host （eggs, larvae, pupae, adult）, host by-products （e.g., frass, exuviae, mandibular gland secretions, defense secretions etc.）, or intra-specific infochemicals （pheromones） can be main signals for the parasitoids. Parasitoids can differentiate between host and non-host, between different hosts and host stages by perceiving specific volatile and contact kairomones from the host itself, host along with its by-product, by-products alone or intra-specific infochemicals; of which frass （by-product） and intra-specific infochemicals are the most reported ones. Adult and larval parasitoids have been reported to be attracted to kairomones of their target stage or byproduct of their host. Pupal parasitoids have been found to utilize kairomones from the preceding host stage while egg parasitoids are known to exploit a variety of host infochemicals, for example, either from eggs themselves or other non-target host stages, especially adults and adult-related by-products. The kairomonal chemicals identified so far include various groups, but mainly hydrocarbons. A high degree of host specificity and host acceptance is important for the parasitoids as any mistake may result in the loss of fitness.     

Insect immune resistance to parasitoids

Insect host-parasitoid interactions involve complex physiological, biochemical and genetic interactions. Against endoparasitoids, immune-competent hosts initiate a blood cell-mediated response that quickly destroys the intruders and envelops them in a multilayered melanotic capsule. During the past decade, considerable progress has been made in identifying some of the critical components of the host response, mainly because of the use of efficient molecular tools. This review examines some of the components of the innate immune response of Drosophila, an insect that has served as an exceptionally good experimental model for studying non-self recognition processes and immune cell signaling mechanisms. Topics considered in this review include hematopoiesis, proliferation and adhesion of hemocytes, melanogenesis and associated cytotoxic molecules, and the genetic aspects of the host-parasitoid interaction.     

拟寄生昆虫中的过寄生现象

对拟寄生昆虫同种过寄生现象做了综述。拟寄生昆虫的认识能力和寄生经历、其与寄主数量的相对比例、寄主的大小及两次被寄生的时间间隔等是导致过寄生是否出现的主要因素。过寄生常导致拟寄生昆虫发育历期延长、存活率下降、个体变小、子代雌性比降低。试验研究和大量饲养中应采取措施避免过寄生。     

Evolutionary costs and benefits of infection with diverse strains of Spiroplasma in pea aphids*

The heritable endosymbiont Spiroplasma infects many insects and has repeatedly evolved the ability to protect its hosts against different parasites. Defenses do not come for free to the host, and theory predicts that more costly symbionts need to provide stronger benefits to persist in host populations. We investigated the costs and benefits of Spiroplasma infections in pea aphids (Acyrthosiphon pisum), testing 12 bacterial strains from three different clades. Virtually all strains decreased aphid lifespan and reproduction, but only two had a (weak) protective effect against the parasitoid Aphidius ervi, an important natural enemy of pea aphids. Spiroplasma‐induced fitness costs were variable, with strains from the most slowly evolving clade reaching higher titers and curtailing aphid lifespan more strongly than other strains. Some Spiroplasma strains shared their host with a second endosymbiont, Regiella insecticola. Although the result of an unfortunate handling error, these co‐infections proved instructive, because they showed that the cost of infection with Spiroplasma may be attenuated in the presence of Regiella. These results suggest that mechanisms other than protection against A. ervi maintain pea aphid infections with diverse strains of Spiroplasma, and that studying them in isolation will not provide a complete picture of their effects on host fitness.