Search

Three related Aphidius parasitoid species share the same host, the grain aphid Sitobion avenae. Among this parasitoid community, Aphidius rhopalosiphi is the most abundant species in the field. Both the interspecific host discrimination of A. rhopalosiphi towards hosts parasitized by the two other species (i.e. A. avenae and A. ervi) and the interspecific host discrimination of the two other species towards hosts parasitized by A. rhopalosiphi were studied here. Results showed that females of A. rhopalosiphi and A. avenae both discriminated between unparasitized hosts and hosts parasitized by the other species. This discrimination occurred only after ovipositor insertion, suggesting the perception of an internal marker of parasitism. Likewise, females of A. rhopalosiphi and A. ervi were able to discriminate between unparasitized hosts and hosts parasitized by the other species. However, in this combination of species, recognition of parasitized hosts occurred before ovipositor insertion, through an antennal perception, suggesting the presence an external cue indicating parasitism. Hence, interspecific host discrimination in the three Aphidius species is based on internal or external cues, which are used either alone or together. Our results showed that the cues used for interspecific host discrimination depend on the specific identity of the interaction. These differences seemed strongly linked to the way the different species respond to defensive behaviours of their aphid hosts. Results are discussed in the context of optimal foraging and possible consequences for community structure. [ABSTRACT FROM AUTHOR]

Transition from sexual reproduction to parthenogenesis constitutes a major life-history change with deep evolutionary consequences for sex-related traits, which are expected to decay. The pea aphid Acyrthosiphon pisum shows intraspecific reproductive polymorphism, with cold-resistant cyclically parthenogenetic (CP) lineages that alternate sexual and asexual generations and cold-sensitive obligately parthenogenetic (OP) lineages that produce only asexual females but still males. Here, the genotyping of 219 pea aphid lineages collected in cold-winter and mild-winter regions revealed contrasting population structures. Samples from cold-winter regions consisted mostly of distinct multilocus genotypes (MLGs) usually represented by a single sample (101 different MLGs for 111 samples) and were all phenotyped as CP. In contrast, fewer MLGs were found in mild-winter regions (28 MLGs for 108 samples), all but one being OP. Since the males produced by OP lineages are unlikely to pass on their genes (sexual females being rare in mild-winter regions), we tested the hypothesis that their traits could degenerate due to lack of selection by comparing male production and male reproductive success between OP and CP lineages. Male production was indeed reduced in OP lineages, but a less clear pattern was observed for male reproductive success: females mated with OP males laid fewer eggs (fertilized or not) but OP and CP males fertilized the same proportion of eggs. These differences may stem from the type of selective forces: male production may be counter-selected whereas male performances may evolve under the slower process of relaxed selection. The overall effective reproductive capacity of OP males could result from recent sex loss in OP lineages or underestimated reproductive opportunities., (© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Compared to open-field crops, the influence of the surrounding landscape on insect diversity in greenhouse crops has been poorly studied. Due to growing evidence of insect influx in greenhouses, identifying the landscape properties influencing the protected crop colonization by insect pests and their natural enemies would promote the improvement of both pest prevention and conservation biological control methods. Here, we present a field study on the effect of the surrounding landscape on the colonization of greenhouse crops by insect pests and associated natural enemies. By monitoring 32 greenhouse strawberry crops in the South West of France, we surveyed crop colonization by four insect pests and four natural enemy groups over two cultivation periods. Our results showed that the landscape structure and composition could have contrasting effects on insect colonization of greenhouse crops so there could be species-specific effects and not general ones. While the degree of openness of greenhouses and the pest management practices modulated insect diversity marginally, we also showed that seasonality represented a key factor in insect crop colonization. The various responses of insect pests and natural enemy groups to the landscape support the idea that pest management methods must involve the surrounding environment.

While ecological interactions have been identified as determinant for biological control efficiency, the role of evolution remains largely underestimated in biological control programs. With the restrictions on the use of both pesticides and exotic biological control agents (BCAs), the evolutionary optimization of local BCAs becomes central for improving the efficiency and the resilience of biological control. In particular, we need to better account for the natural processes of evolution to fully understand the interactions of pests and BCAs, including in biocontrol strategies integrating human manipulations of evolution (i.e., artificial selection and genetic engineering). In agroecosystems, the evolution of BCAs traits and performance depends on heritable phenotypic variation, trait genetic architecture, selection strength, stochastic processes, and other selective forces. Humans can manipulate these natural processes to increase the likelihood of evolutionary trait improvement, by artificially increasing heritable phenotypic variation, strengthening selection, controlling stochastic processes, or overpassing evolution through genetic engineering. We highlight these facets by reviewing recent studies addressing the importance of natural processes of evolution and human manipulations of these processes in biological control. We then discuss the interactions between the natural processes of evolution occurring in agroecosystems and affecting the artificially improved BCAs after their release. We emphasize that biological control cannot be summarized by interactions between species pairs because pests and biological control agents are entangled in diverse communities and are exposed to a multitude of deterministic and stochastic selective forces that can change rapidly in direction and intensity. We conclude that the combination of different evolutionary approaches can help optimize BCAs to remain efficient under changing environmental conditions and, ultimately, favor agroecosystem sustainability., Competing Interests: The authors have no conflicts of interest to declare., (© 2022 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd.)

Ecological specialization is widespread in animals, especially in phytophagous insects, which have often a limited range of host plant species. This host plant specialization results from divergent selection on insect populations, which differ consequently in traits like behaviors involved in plant use. Although recent studies highlighted the influence of symbionts on dietary breadth of their insect hosts, whether these microbial partners influence the foraging capacities of plant-specialized insects has received little attention. In this study, we used the pea aphid Acyrthosiphon pisum, which presents distinct plant-specialized lineages and several secondary bacterial symbionts, to examine the possible effects of symbionts on the different foraging steps from plant searching to host plant selection. In particular, we tested the effect of secondary symbionts on the aphid capacity (1) to explore habitat at long distance (estimated through the production of winged offspring), (2) to explore habitat at short distance, and (3) to select its host plant. We found that secondary symbionts had a variable influence on the production of winged offspring in some genotypes, with potential consequences on dispersal and survival. By contrast, symbionts influenced both short-distance exploration and host plant selection only marginally. The implication of symbionts' influence on insect foraging capacities is discussed., (© 2021. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.)

Due to their ability to parasitize various insect species, generalist parasitoids are widely used as biological control agents. They can be mass-reared and released in agroecosystems to control several pest species in various crops. However, the existence of genetic differentiation among populations of generalist parasitoid species is increasingly recognized and this can be associated with an adaptation to local conditions or to a reduced range of host species. Moreover, constraints of mass-rearing conditions can alter genetic variation within parasitoid populations released. These features could be associated with a reduced efficiency of the control of targeted pest species. Here, we focused on strawberry greenhouses where the control of aphids with the generalist parasitoid Aphidius ervi appears to be inefficient. We investigated whether this inefficiency may have both genetic and ecological bases comparing wild and commercial populations of A. ervi. We used two complementary genetic approaches: one based on the mitochondrial marker COI and one based on microsatellite markers. COI analysis showed a genetic differentiation within the A. ervi species, but the structure was neither associated with the commercial/wild status nor with host species factors. On the other hand, using microsatellite markers, we showed a genetic differentiation between commercial and wild A. ervi populations associated with a loss of genetic diversity within the mass-reared populations. Our ecological genetics study may potentially explain the weak efficiency of biological control of aphids in protected strawberry crops and enable to provide some insights to improve biological control., Competing Interests: The authors have declared that no competing interests exist.

Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa , a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.

Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e., from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum , and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid-symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola , two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid-symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host-parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect-symbiont associations., (© The Author(s) (2020). Published by Oxford University Press on behalf of Editorial Office, Current Zoology.)

Insect symbionts benefit their host and their study requires large spectrum antibiotic use like tetracycline to weaken or suppress symbiotic communities. While antibiotics have a negative impact on insect fitness, little is known about antibiotic effects on insect microbial communities and how long they last. We characterized the bacterial communities of adult cabbage root fly Delia radicum in a Wolbachia-free population and evaluated the effect of tetracycline treatment on these communities over several generations. Three D. radicum generations were used: the first- and second-generation flies either ingested tetracycline or not, while the third-generation flies were untreated but differed with their parents and/or grandparents that had or had not been treated. Fly bacterial communities were sequenced using a 16S rRNA gene. Tetracycline decreased fly bacterial diversity and induced modifications in both bacterial abundance and relative frequencies, still visible on untreated offspring whose parents and/or grandparents had been treated, therefore demonstrating long-lasting transgenerational effects on animal microbiomes after antibiotic treatment. Flies with an antibiotic history shared bacterial genera, potentially tetracycline resistant and heritable. Next, the transmission should be investigated by comparing several insect development stages and plant compartments to assess vertical and horizontal transmissions of D. radicum bacterial communities., (© FEMS 2020.)

Arctic ecosystems are subjected to strong environmental constraints that prevent both the colonization and development of many organisms. In Svalbard, few aphid species have established permanent populations. These high arctic aphid species have developed peculiar life-history traits such as shortened life cycles and reduced dispersal capacities. Here, we present data on the distribution and population genetics of Acyrthosiphon svalbardicum in Spitsbergen, the main island of the Svalbard archipelago, and compared its genetic structure with that of its close relative Acyrthosiphon brevicorne, sampled in the top of Scandinavian mainland. We found that A. svalbardicum is common but heterogeneously distributed along the west coast of Spitsbergen. We recorded this species up to 79°12', which constitutes the northernmost location for any aphid. Genetic structure examined using microsatellite markers showed more pronounced spatial differentiation in A. svalbardicum than in A. brevicorne populations, presumably due to reduced dispersal capacities in the former species. Although populations of A. brevicorne and A. svalbardicum were well-delineated at nuclear loci, they shared similar cytoplasmic DNA haplotypes as revealed by sequence analysis of two DNA barcodes. These results raise questions about whether these two taxa are different species, and the colonization sources and history of the Svalbard archipelago by A. svalbardicum .

In insects, bacterial endosymbionts are known to influence the ecology of their hosts by modifying interactions with natural enemies such as parasitoids. Symbionts can modulate both parasitoid behavioral and/or physiological traits as well as host behaviors and life-history traits. Together these suggest that endosymbionts may impact the host range of parasitoids. For example, endosymbionts may narrow parasitoid host range through first, reducing parasitoid ability to locate hosts and/or larval survival, second, affecting fitness traits of the emerging adult parasitoid and/or third, modulating the outcome of interference and exploitative competition between parasitoid species. From both a fundamental and applied point of view, these symbiotic effects would influence the ecology and evolution of parasitoids and associated population-level processes and ecosystem services (e.g. biocontrol)., (Copyright © 2018. Published by Elsevier Inc.)

Symbiotic associations between microbes and insects are widespread, and it is frequent that several symbionts share the same host individual. Hence, interactions can occur between these symbionts, influencing their respective abundance within the host with consequences on its phenotype. Here, we investigate the effects of multiple infections in the pea aphid, Acyrthosiphon pisum, which is the host of an obligatory and several facultative symbionts. In particular, we study the influence of a coinfection with 2 protective symbionts: Hamiltonella defensa, which confers protection against parasitoids, and Rickettsiella viridis, which provides protection against fungal pathogens and predators. The effects of Hamiltonella-Rickettsiella coinfection on the respective abundance of the symbionts, host fitness and efficacy of enemy protection were studied. Asymmetrical interactions between the 2 protective symbionts have been found: when they coinfect the same aphid individuals, the Rickettsiella infection affected Hamiltonella abundance within hosts but not the Hamiltonella-mediated protective phenotype while the Hamiltonella infection negatively influences the Rickettsiella-mediated protective phenotype but not its abundance. Harboring the 2 protective symbionts also reduced the survival and fecundity of host individuals. Overall, this work highlights the effects of multiple infections on symbiont abundances and host traits that are likely to impact the maintenance of the symbiotic associations in natural habitats., (© 2016 Institute of Zoology, Chinese Academy of Sciences.)

All animals are infected by microbial partners that can be passengers or residents and influence many biological traits of their hosts. Even if important factors that structure the composition and abundance of microbial communities within and among host individuals have been recently described, such as diet, developmental stage or phylogeny, few studies have conducted cross-taxonomic comparisons, especially on host species related by trophic relationships. Here, we describe and compare the microbial communities associated with the cabbage root fly Delia radicum and its three major parasitoids: the two staphylinid beetles Aleochara bilineata and A. bipustulata and the hymenopteran parasitoid Trybliographa rapae. For each species, two populations from Western France were sampled and microbial communities were described through culture independent methods (454 pyrosequencing). Each sample harbored at least 59 to 261 different bacterial phylotypes but was strongly dominated by one or two. Microbial communities differed markedly in terms of composition and abundance, being mainly influenced by phylogenetic proximity but also geography to a minor extent. Surprisingly, despite their strong trophic interaction, parasitoids shared a very low proportion of microbial partners with their insect host. Three vertically transmitted symbionts from the genus Wolbachia, Rickettsia, and Spiroplasma were found in this study. Among them, Wolbachia and Spiroplasma were found in both the cabbage fly and at least one of its parasitoids, which could result from horizontal transfers through trophic interactions. Phylogenetic analysis showed that this hypothesis may explain some but not all cases. More work is needed to understand the dynamics of symbiotic associations within trophic network and the effect of these bacterial communities on the fitness of their hosts.

The rise of temperatures may enable species to increase their activities during winter periods and to occupy new areas. In winter, resource density is low for most species and an increased number of active consumers during this season may produce heightened competitive pressure. In Western France, the aphid parasitoid species Aphidius avenae Haliday has been known to adopt a winter diapausing strategy adjacent to newly sown cereal crops, until recent reports of active winter populations in cereal crops. We investigate how the addition of this species to the winter guild of parasitoids may change the structure of the aphid-parasitoid food web and the host-exploitation strategies of previously occurring parasitoids. We showed that in winter, Aphidius avenae was mostly associated with two aphid species, Sitobion avenae Fabricius and Metopolophium dirhodum Walker, while the generalist species Aphidius rhopalosiphi was restricted to the aphid species Rhopalosiphum padi L. in the presence of Aphidius avenae. Due to this new competition, winter food webs present a higher degree of compartmentalization and lower proportional similarity index values than spring ones. Parasitoid and aphid abundances responded significantly to changes in daily high temperatures, suggesting that the host-parasitoid community structure can be partly predicted by climate. This study demonstrates how a change in the winter strategy of one species of a guild can modify complex interspecific relationships in host-parasitoid systems.

Symbionts are widespread among eukaryotes and their impacts on the ecology and evolution of their hosts are meaningful. Most insects harbour obligate and facultative symbiotic bacteria that can influence their phenotype. In the pea aphid Acyrthosiphon pisum, an astounding symbiotic-mediated phenotype has been recently observed: when infected with the symbiotic bacteria Rickettsiella viridis, young red aphid larvae become greener at adulthood and even darker green when co-infected with Rickettsiella viridis and Hamiltonella defensa. As body colour affects the susceptibility towards natural enemies in aphids, the influence of the colour change due to these facultative symbionts on the host survival in presence of predators was tested. Our results suggested that the Rickettsiella viridis infection may impact positively host survival by reducing predation risk. Due to results from uninfected aphids (i.e., more green ones attacked), the main assumption is that this symbiotic infection would deter the predatory ladybird feeding by reducing the profitability of their hosts rather than decreasing host detection through body colour change. Aphids co-infected with Rickettsiella viridis and Hamiltonella defensa were, however, more exposed to predation suggesting an ecological cost associated with multiple infections. The underlying mechanisms and ecological consequences of these symbiotic effects are discussed.

Host recognition and use in female parasitoids strongly relies on host fidelity, a plastic behavior which can significantly restrict the host preferences of parasitoids, thus reducing the gene flow between parasitoid populations attacking different insect hosts. However, the effect of migrant males on the genetic differentiation of populations has been frequently ignored in parasitoids, despite its known impact on gene flow between populations. Hence, we studied the extent of gene flow mediated by female and male parasitoids by assessing sibship relationships among parasitoids within and between populations, and its impact on geographic and host-associated differentiation in the aphid parasitoid Aphidius ervi. We report evidences of a high gene flow among parasitoid populations on different aphid hosts and geographic locations. The high gene flow among parasitoid populations was found to be largely male mediated, suggested by significant differences in the distribution of full-sib and paternal half-sib dyads of parasitoid populations.

Associations between microbes and animals are ubiquitous and hosts may benefit from harbouring microbial communities through improved resource exploitation or resistance to environmental stress. The pea aphid, Acyrthosiphon pisum, is the host of heritable bacterial symbionts, including the obligate endosymbiont Buchnera aphidicola and several facultative symbionts. While obligate symbionts supply aphids with key nutrients, facultative symbionts influence their hosts in many ways such as protection against natural enemies, heat tolerance, color change and reproduction alteration. The pea aphid also encompasses multiple plant-specialized biotypes, each adapted to one or a few legume species. Facultative symbiont communities differ strongly between biotypes, although bacterial involvement in plant specialization is uncertain. Here, we analyse the diversity of bacterial communities associated with nine biotypes of the pea aphid complex using amplicon pyrosequencing of 16S rRNA genes. Combined clustering and phylogenetic analyses of 16S sequences allowed identifying 21 bacterial OTUs (Operational Taxonomic Unit). More than 98% of the sequencing reads were assigned to known pea aphid symbionts. The presence of Wolbachia was confirmed in A. pisum while Erwinia and Pantoea, two gut associates, were detected in multiple samples. The diversity of bacterial communities harboured by pea aphid biotypes was very low, ranging from 3 to 11 OTUs across samples. Bacterial communities differed more between than within biotypes but this difference did not correlate with the genetic divergence between biotypes. Altogether, these results confirm that the aphid microbiota is dominated by a few heritable symbionts and that plant specialization is an important structuring factor of bacterial communities associated with the pea aphid complex. However, since we examined the microbiota of aphid samples kept a few generations in controlled conditions, it may be that bacterial diversity was underestimated due to the possible loss of environmental or transient taxa.

Linking adaptive divergence to hybrid unfitness is necessary to understand the ecological factors contributing to reproductive isolation and speciation. To date, this link has been demonstrated in few model systems, most of which encompass ecotypes that occupy relatively early stages in the speciation process. Here we extend these studies by assessing how host-plant adaptation conditions hybrid fitness in the pea aphid, Acyrthosiphon pisum. We made crosses between and within five pea aphid biotypes adapted to different host plants and representing various stages of divergence within the complex. Performance of F1 hybrids and nonhybrids was assessed on a "universal" host that is favorable to all pea aphid biotypes in laboratory conditions. Although hybrids performed equally well as nonhybrids on the universal host, their performance was much lower than nonhybrids on the natural hosts of their parental populations. Hence, hybrids, rather than being intrinsically deficient, are maladapted to their parents' hosts. Interestingly, the impact of this maladaptation was stronger in certain hybrids from crosses involving the most divergent biotype, suggesting that host-dependent postzygotic isolation has continued to evolve late in divergence. Even though host-independent deficiencies are not excluded, hybrid maladaptation to parental hosts supports the hypothesis of ecological speciation in this complex., (© 2014 The Author(s). Evolution © 2014 The Society for the Study of Evolution.)

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called "direct costs", arise from a trade-off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont-mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont-free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.

Aphids harbour both an obligate bacterial symbiont, Buchnera aphidicola, and a wide range of facultative ones. Facultative symbionts can modify morphological, developmental and physiological host traits that favour their spread within aphid populations. We experimentally investigated the idea that symbionts may also modify aphid behavioural traits to enhance their transmission. Aphids exhibit many behavioural defences against enemies. Despite their benefits, these behaviours have some associated costs leading to reduction in aphid reproduction. Some aphid individuals harbour a facultative symbiont Hamiltonella defensa that provides protection against parasitoids. By analysing aphid behaviours in the presence of parasitoids, we showed that aphids infected with H. defensa exhibited reduced aggressiveness and escape reactions compared with uninfected aphids. The aphid and the symbiont have both benefited from these behavioural changes: both partners reduced the fitness decrements associated with the behavioural defences. Such symbiont-induced changes of behavioural defences may have consequences for coevolutionary processes between host organisms and their enemies.

Some bacterial symbionts alter their hosts reproduction through various mechanisms that enhance their transmission in the host population. In addition to its obligatory symbiont Buchnera aphidicola, the pea aphid Acyrthosiphon pisum harbors several facultative symbionts influencing several aspects of host ecology. Aphids reproduce by cyclical parthenogenesis whereby clonal and sexual reproduction alternate within the annual life cycle. Many species, including the pea aphid, also show variation in their reproductive mode at the population level, with some lineages reproducing by cyclical parthenogenesis and others by permanent parthenogenesis. While the role of facultative symbionts has been well studied during the parthenogenetic phase of their aphid hosts, very little is known on their possible influence during the sexual phase. Here we investigated whether facultative symbionts modulate the capacity to produce sexual forms in various genetic backgrounds of the pea aphid with controlled symbiont composition and also in different aphid genotypes from natural populations with previously characterized infection status and reproductive mode. We found that most facultative symbionts exhibited detrimental effects on their hosts fitness under sex-inducing conditions in comparison with the reference lines. We also showed that the loss of sexual phase in permanently parthenogenetic lineages of A. pisum was not explained by facultative symbionts. Finally, we demonstrated that Spiroplasma infection annihilated the production of males in the host progeny by inducing a male-killing phenotype, an unexpected result for organisms such as aphids that reproduce primarily through clonal reproduction.

Many organisms, including entomopathogenous fungi, predators or parasites, use aphids as ressources. Parasites of aphids are mostly endoparasitoid insects, i.e. insects which lay eggs inside the body of an other insect which will die as a result of their development. In this article, we review the consequences of the numerous pecularities of aphid biology and ecology for their endoparasitoids, notably the Aphidiinae (Hymenoptera: Braconidae). We first examine the various mechanisms used by aphids for defence against these enemies. We then explore the strategies used by aphidiine parasitoids to exploit their aphid hosts. Finally, we consider the responses of both aphids and parasitoids to ecological constraints induced by seasonal cycles and to environmental variations linked to host plants and climate. The fundamental and applied interest of studying these organisms is discussed., (Copyright 2010 Académie des sciences. Published by Elsevier SAS. All rights reserved.)

In 2009, the genome of the pea aphid (Acyrthosiphon pisum) was sequenced and partially annotated. This means that the scientific community has now access to the genetic material of aphids that are serious pests of plants. The description of an aphid genome is a first step to go deeper in the understanding of the biology of these insects. In this article, we first describe how the pea aphid genome has been sequenced and its major characteristics. However, a genome is only a part of what an individual is and describing a genome without taking into account the role of the environment makes no sense. Thus, in the second part of the review, we envisage how this genomic resource will fuel many other disciplines such as ecology, evolutionary biology, population genetics and symbiosis., (Copyright 2010 Académie des sciences. Published by Elsevier SAS. All rights reserved.)

Background: Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. Altruistic behaviours can evolve through indirect fitness benefits when directed toward kin. The altruistic nature of anti-predatory behaviours is often difficult to establish because the actor can obtain direct fitness benefits, or the behaviour could result from selfish coercion by others, especially in eusocial animals. Non-eusocial parthenogenetically reproducing aphids form colonies of clone-mates, which are ideal to test the altruistic nature of anti-predatory defence behaviours. Many aphids release cornicle secretions when attacked by natural enemies such as parasitoids. These secretions contain an alarm pheromone that alerts neighbours (clone-mates) of danger, thereby providing indirect fitness benefits to the actor. However, contact with cornicle secretions also hampers an attacker and could provide direct fitness to the actor., Results: We tested the hypothesis that cornicle secretions are altruistic by assessing direct and indirect fitness consequences of smearing cornicle secretions onto an attacker, and by manipulating the number of clone-mates that could benefit from the behaviour. We observed parasitoids, Aphidius rhopalosiphi, foraging singly in patches of the cereal aphid Sitobion avenae of varied patch size (2, 6, and 12 aphids). Aphids that smeared parasitoids did not benefit from a reduced probability of parasitism, or increase the parasitoids' handling time. Smeared parasitoids, however, spent proportionately more time grooming and less time foraging, which resulted in a decreased host-encounter and oviposition rate within the host patch. In addition, individual smearing rate increased with the number of clone-mates in the colony., Conclusions: Cornicle secretions of aphids were altruistic against parasitoids, as they provided no direct fitness benefits to secretion-releasing individuals, only indirect fitness benefits through neighbouring clone-mates. Moreover, the use of cornicle secretions was consistent with their altruistic nature, because the occurrence of this behaviour increased with the size of indirect fitness benefits, the number of clone-mates that can benefit. This study provides evidence for a case of kin-directed altruistic defence outside eusocial animals.

Current models in evolutionary ecology predict life history alterations in response to habitat suitability to optimize fitness. Only few empirical studies have demonstrated how life history traits that are expected to trade off against each other differ among environments. In Europe, many salt marshes have been recently invaded by the grass Elymus athericus. Previous studies however showed higher densities of the endangered spider Arctosa fulvolineata (Araneae: Lycosidae) in invaded salt marshes compared to natural habitats, which suggests a lower habitat suitability in the latter. The aim of this study was to determine if this emerging habitat (1) affects the amount of resource acquisition and (2) alters the balance between life history traits that are expected to trade off against each other in this stenotopic salt marsh species. As suggested by theoretical studies, an optimization of fitness by increasing egg size at the cost of decreasing fecundity in unsuitable (i.e., natural) habitats was expected. Females presenting cocoon were then collected in close invaded and natural salt marsh areas within the Mont Saint-Michel Bay (France). By considering female mass as covariate, cocoon mass, number of eggs, and egg volume were compared between both habitats. Clutch mass was strongly determined by female mass in both habitats. Clutch mass was however significantly smaller in the natural habitat compared to the invaded habitat, indicating a higher resource acquisition in the latter. When correcting for female size, fecundity was additionally increased in the invaded habitat through a significant decrease in egg size. This phenotypic response can be explained by differences in habitat structure between invaded and natural habitats: the former offers a more complex litter favoring nocturnal wanderers like A. fulvolineata. The existence of such an adaptive reproduction strategy depending on habitat suitability constitutes an original case of an invasion that favors an endangered species.

Changes in the genetic structure and genotypic variation of the aphid Sitobion avenae collected from cereal crops in northern France were examined by analysing variation at five microsatellite loci across several years and seasons. Little regional and temporal differentiation was detected, as shown by very low FST among populations. Repeated genotypes, significant heterozygote deficits, positive FIS values and frequent linkage disequilibria were found in nearly all samples, suggesting an overall pattern of reproductive mode variation in S. avenae populations. In addition, samples from Brittany (Bretagne) showed greater signs of asexual reproduction than those from the north of France, indicating a trend toward increasing sexuality northward. These patterns of reproductive variation in S. avenae are consistent with theoretical models of selection of aphid reproductive modes by climate. Contrasting with little changes in allelic frequencies, genotypic composition varied substantially in time and, to a lesser extent, in space. An important part of changes in genotypic arrays was due to the variation in frequency distribution of common genotypes, i.e. those that were found at several instances in the samples. Genotypic composition was also shown to vary according to climate, as genotypic diversity in spring was significantly correlated with the severity of the previous winter and autumn. We propose that the genetic homogeneity among S. avenae populations shown here across large temporal and spatial scales is the result of two forces: (i) migration conferred by high dispersal capabilities, and (ii) selection over millions of hectares of cereals (mostly wheat) bred from a narrow genetic base.

The distribution of parasites within host natural populations has often been found to be host age-dependent. Host mortality induced by parasites is the commonest hypothesis proposed for explaining this pattern. Despite its potential importance in ecology, the parasitism intensity in relation with the host age has rarely been studied in the field. The 2 manipulative acanthocephalans, Polymorphus minutus and Pomphorhynchus laevis, use the amphipod Gammarus pulex as an intermediate host, and their infection intensity and incidence among G. pulex populations were examined by analyzing 2 large samples of hosts collected in eastern France. Both parasites had low prevalence in the host populations, but their mean abundances were highly related with gammarid age. For the 2 acanthocephalans, results reported a disappearance or an absence of heavily infected hosts in the older host age classes. These results suggested that parasites that alter intermediate host behavior for enhancing their transmission success to the definitive host reduce the survival of their intermediate host. In conclusion, manipulative parasites might act as a mechanism regulating the density of gammarid populations.

Host acceptance decision in parasitic wasps strongly depends on the parasitism status of the encountered host. In solitary species, a host only allows the development of a single parasitic larva and then, any oviposition in an already parasitised host leads to larval competition and loss of offspring. Females of many parasitoid species are able to discriminate between parasitised hosts and healthy ones. However, the host discrimination process may require more time than oviposition, exposing the wasp to high risks when the host has efficient defences. Consequently, depending on the degree of success of the host defence, the cost of host inspection for discrimination can outweigh the benefit of superparasitism avoidance. In the present paper, a theoretical approach was developed for determining how host defences may affect optimal host acceptance behaviour in parasitoids. The present model compares the lifetime reproductive success over the strategy used, discrimination and no-discrimination: a discriminating wasp sets a relatively greater value in its current oviposition, while a non-discriminating female sets a greater value in its own survival and future reproduction. The model predicts that depending on physiological state variables and environmental state variables, the optimal policy is not discriminating. Our results suggest that the low discriminating ability observed in some parasitic wasps could probably be an evolutionary response to host defences pressure.

For many parasites with complex life cycles, manipulation of intermediate host phenotypes is often regarded as an adaptation to increase the probability of successful transmission. This phenomenon creates opportunities for either synergistic or conflicting interests between different parasite species sharing the same intermediate host. When more than one manipulative parasite infect the same intermediate host, but differ in their definitive host, selection should favour the establishment of a negative association between these manipulators. Both Polymorphus minutus and Pomphorhynchus laevis exploit the amphipod Gammarus pulex as intermediate host but differ markedly in their final host, a fish for P. laevis and a bird for P. minutus. The pattern of host use by these two conflicting manipulative parasites was studied. Their incidence and intensity of infection and their distribution among G. pulex were first examined by analysing three large samples of gammarids collected from the river Tille, Eastern France. Both parasites had low prevalence in the host population. However, temporal fluctuation in the level of parasitic infection was observed. Overall, prevalence of both parasite species was higher in male than in female G. pulex. We then assessed the degree of association between the two parasites among their intermediate hosts, using two different methods: a host-centred measure and a parasite-centred measure. Both measures gave similar results; showing random association between the two acanthocephalan species in their intermediate hosts. We discuss our results in relation to the selective forces and ecological constraints that may determine the pattern of association between conflicting manipulative parasites.