Genetic Control of Contagious Asexuality in the Pea Aphid

Although evolutionary transitions from sexual to asexual reproduction are frequent in eukaryotes, the genetic bases of such shifts toward asexuality remain largely unknown. We addressed this issue in an aphid species where both sexual and obligate asexual lineages coexist in natural populations. These sexual and asexual lineages may occasionally interbreed because some asexual lineages maintain a residual production of males potentially able to mate with the females produced by sexual lineages. Hence, this species is an ideal model to study the genetic basis of the loss of sexual reproduction with quantitative genetic and population genomic approaches. Our analysis of the co-segregation of ∼300 molecular markers and reproductive phenotype in experimental crosses pinpointed an X-linked region controlling obligate asexuality, this state of character being recessive. A population genetic analysis (>400-marker genome scan) on wild sexual and asexual genotypes from geographically distant populations under divergent selection for reproductive strategies detected a strong signature of divergent selection in the genomic region identified by the experimental crosses. These population genetic data confirm the implication of the candidate region in the control of reproductive mode in wild populations originating from 700 km apart. Patterns of genetic differentiation along chromosomes suggest bidirectional gene flow between populations with distinct reproductive modes, supporting contagious asexuality as a prevailing route to permanent parthenogenesis in pea aphids. This genetic system provides new insights into the mechanisms of coexistence of sexual and asexual aphid lineages.     

A sex-linked locus controls wing polymorphism in males of the pea aphid,Acyrthosiphon pisum (Harris)

Discrete variation in wing morphology is a very common phenomenon in insects and has been used extensively in the past 50 years as a model to study the ecology and evolution of dispersal. Wing morph determination can be purely genetic, purely environmental, or some combination of the two. The precise genetic determinants of genetically based wing morph variation are unknown. Here we explore the genetic basis of wing polymorphism in the pea aphid, which can produce either winged or wingless males. We confirm that three types of pea aphid clones coexist in natural populations, those producing winged males only, those producing wingless males only, and those producing a mixture of both. A Mendelian genetic analysis reveals that male wing polymorphism in pea aphids is determined by a single locus, two alleles system. Using microsatellite loci of known location, we show that this locus is on the X chromosome. The existence of a simple genetic determinism for wing polymorphism in a system in which genetic investigation is possible may help investigations on the physiological and molecular mechanisms of genetically-based wing morph variation. This locus could also be used in the search for genes involved in the wing polyphenism described in parthenogenetic females and to investigate the interplay between polymorphisms and polyphenisms.     

Genome scans reveal candidate regions involved in the adaptation to host plant in the pea aphid complex

A major goal in evolutionary biology is to uncover the genetic basis of adaptation. Divergent selection exerted on ecological traits may result in adaptive population differentiation and reproductive isolation and affect differentially the level of genetic divergence along the genome. Genome‐wide scan of large sets of individuals from multiple populations is a powerful approach to identify loci or genomic regions under ecologically divergent selection. Here, we focused on the pea aphid, a species complex of divergent host races, to explore the organization of the genomic divergence associated with host plant adaptation and ecological speciation. We analysed 390 microsatellite markers located at variable distances from predicted genes in replicate samples of sympatric populations of the pea aphid collected on alfalfa, red clover and pea, which correspond to three common host‐adapted races reported in this species complex. Using a method that accounts for the hierarchical structure of our data set, we found a set of 11 outlier loci that show higher genetic differentiation between host races than expected under the null hypothesis of neutral evolution. Two of the outliers are close to olfactory receptor genes and three other nearby genes encoding salivary proteins. The remaining outliers are located in regions with genes of unknown functions, or which functions are unlikely to be involved in interactions with the host plant. This study reveals genetic signatures of divergent selection across the genome and provides an inventory of candidate genes responsible for plant specialization in the pea aphid, thereby setting the stage for future functional studies.     

Aphid population dynamics: does resistance to parasitism influence population size?

1. Insect population size is regulated by both intrinsic traits of organisms and extrinsic factors. The impacts of natural enemies are typically considered to be extrinsic factors, however insects have traits that affect their vulnerability to attack by natural enemies, and thus intrinsic and extrinsic factors can interact in their effects on population size. 2. Pea aphids Acyrthosiphon pisum Harris (Hemiptera: Aphididae) in New York and Maryland that are specialised on alfalfa are approximately two times more physiologically resistant to parasitism by Aphidius ervi Haliday (Hymenoptera: Braconidae) than pea aphids specialised on clover. To assess the potential influence of this genetically based difference in resistance to parasitism on pea aphid population dynamics, pea aphids, A. ervi, and other natural enemies of aphids in clover and alfalfa fields were sampled. 3. Rates of successful parasitism by A. ervi were higher and pea aphid population sizes were lower in clover, where the aphids are less resistant to parasitism. In contrast, mortality due to a fungal pathogen of pea aphids was higher in alfalfa. Generalist aphid predators did not differ significantly in density between the crops. 4. To explore whether intrinsic resistance to parasitism influences field dynamics, the relationship between resistance and successful field parasitism in 12 populations was analysed. The average level of resistance of a population strongly predicts rates of successful parasitism in the field. The ability of the parasitoid to regulate the aphid may vary among pea aphid populations of different levels of resistance.     

Effects of a simple plant morphological mutation on the arthropod community and the impacts of predators on a principal insect herbivore

Plant features that enhance predator effectiveness can be considered extrinsic-resistance factors because they result in reduced insect herbivory. In this paper we test the hypothesis that reduced epicuticular wax (EW) in Pisum sativum L. is an extrinsic-resistance factor contributing to field resistance to Acyrthosiphon pisum (Harris). We monitored pea aphid populations in the field on reduced EW and normal EW near isolines of peas for two seasons and confirmed that aphid populations are lower on reduced EW peas than on normal EW peas. We also monitored predators within the canopies of the two pea lines to discover community level patterns in response to differences in EW. We found that while predator numbers were similar between the two lines, there were more syrphids on the normal EW peas, and a trend towards more coccinellids on reduced EW peas. We tested the impact of predators on pea aphids on the two EW lines by monitoring their population levels in cages that excluded predators, and in cages that allowed predators to enter. We found that pea aphid populations were similar on the two EW lines when predators were excluded. When predators were allowed access to the plants, pea aphid populations were reduced more on reduced EW peas than on normal EW peas. We also examined the intrinsic resistance to aphids in reduced EW peas with laboratory dual-choice tests comparing aphid response to reduced EW and normal EW peas, and found that walking, apterous aphids displayed no preference for one pea line over the other. Bioassays to measure growth and fecundity of the pea aphid on the two EW types in the greenhouse and in the field showed that intrinsic rate of increase, and other life table parameters, were not different for aphids on the two lines. Together these results support the hypothesis that reduced EW in peas is a predator-dependent extrinsic resistance factor. Genetically reducing EW bloom in peas and other waxy crop plants might improve the effectiveness of arthropod natural enemies of insect pests. More generally, the results show that a subtle change in plant morphology can substantially influence the impact of predators on insect herbivore populations. The benefit of extrinsic resistance to herbivory conferred by reduced EW may balance any benefits of a prominent EW bloom, thereby sustaining EW polymorphisms in some natural plant populations.     

Identifying genomic hotspots of differentiation and candidate genes involved in the adaptive divergence of pea aphid host races

Identifying the genomic bases of adaptation to novel environments is a long‐term objective in evolutionary biology. Because genetic differentiation is expected to increase between locally adapted populations at the genes targeted by selection, scanning the genome for elevated levels of differentiation is a first step towards deciphering the genomic architecture underlying adaptive divergence. The pea aphid Acyrthosiphon pisum is a model of choice to address this question, as it forms a large complex of plant‐specialized races and cryptic species, resulting from recent adaptive radiation. Here, we characterized genomewide polymorphisms in three pea aphid races specialized on alfalfa, clover and pea crops, respectively, which we sequenced in pools (poolseq). Using a model‐based approach that explicitly accounts for selection, we identified 392 genomic hotspots of differentiation spanning 47.3 Mb and 2,484 genes (respectively, 9.12% of the genome size and 8.10% of its genes). Most of these highly differentiated regions were located on the autosomes, and overall differentiation was weaker on the X chromosome. Within these hotspots, high levels of absolute divergence between races suggest that these regions experienced less gene flow than the rest of the genome, most likely by contributing to reproductive isolation. Moreover, population‐specific analyses showed evidence of selection in every host race, depending on the hotspot considered. These hotspots were significantly enriched for candidate gene categories that control host–plant selection and use. These genes encode 48 salivary proteins, 14 gustatory receptors, 10 odorant receptors, five P450 cytochromes and one chemosensory protein, which represent promising candidates for the genetic basis of host–plant specialization and ecological isolation in the pea aphid complex. Altogether, our findings open new research directions towards functional studies, for validating the role of these genes on adaptive phenotypes.     

Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation

Variation in traits affecting preference for, and performance on, new habitats is a key factor in the initiation of ecological specialisation and adaptive speciation. However, habitat and resource use also involves other traits whose influence on ecological and genetic divergence remains poorly understood. In the present study, we investigated the extent of variation of life-history traits among sympatric populations of the pea aphid Acyrthosiphon pisum , which shows several host races that are specialised on various plants of the family Fabaceae plants and is an established model for ecological speciation. First, we assessed the community structure of microbial partners within host populations of the pea aphid. The effect of these microbes on host fitness is uncertain, although there is growing evidence that they may modulate various important adaptive traits of their host such as plant utilisation and resistance against natural enemies. Second, we performed a multivariate analysis on several ecologically relevant features of host populations recorded in the present and previous studies (including microbial composition, colour morph, reproductive mode, and male dispersal phenotype), enabling the identification of correlations between phenotypic traits. We discuss the ecological significance of these associations of traits in relation to the habitat characteristics of pea aphid populations, and their consequences for the evolution of ecological specialisation and sympatric speciation.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 718–727.     

Intraguild interactions of aphidophagous predators in fields: effect of Coccinella septempunctata and Episyrphus balteatus occurrence on aphid infested plants

Intraguild relations between beneficial insects have become a major research topic in biological pest control. In order to understand the intraguild competitions between aphidophagous populations in natural conditions, a field experiment was carried out in the experimental farm of the Gembloux Agricultural University. As biological control of pests involve a community of diverse natural enemies, this experiment firstly aimed to assess the aphidophagous predator diversity and abundance in green pea (Pisum sativum) field and secondly to investigate the impact of the large natural occurrence of C. septempunctata on the aphidophagous beneficial dispersion and efficiency as aphid biological control agents in pea field. Visual observations were weekly performed throughout the 2006 growing season. The pea aphids were attacked by several predatory groups, mainly ladybird beetles and hoverflies. Higher densities of ladybirds and hoverflies were recorded in the beginning of July, associated with an aphid occurrence peak. Using net cage system in the field, the particular intraguild relations between added C. septempunctata or E. balteatus and the natural beneficial arrivals and dispersion were observed. The E. batteatus (eggs and larvae) presence inhibited other aphidophagous predators presence on the aphid infested plants. Lower abundance of E. balteatus was observed on aphid infested plants already colonised by C. septempunctata. To explore more accurately the oviposition and predation behaviours of ladybirds and hoverflies and to determine the chemical factors that could influence these behaviours, current researches are performed in laboratory and will be discussed to promote efficient biological control of aphids by natural enemies.     

Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera

In natural populations of the pea aphid Acyrthosiphon pisum, a facultative bacterial symbiont of the genus Rickettsia has been detected at considerable infection frequencies worldwide. We investigated the effects of the Rickettsia symbiont on the host aphid and also on the coexisting essential symbiont Buchnera. In situ hybridization revealed that the Rickettsia symbiont was specifically localized in two types of host cells specialized for endosymbiosis: secondary mycetocytes and sheath cells. Electron microscopy identified bacterial rods, about 2 mum long and 0.5 mum thick, in sheath cells of Rickettsia-infected aphids. Virus-like particles were sometimes observed in association with the bacterial cells. By an antibiotic treatment, we generated Rickettsia-infected and Rickettsia-eliminated aphid strains with an identical genetic background. Comparison of these strains revealed that Rickettsia infection negatively affected some components of the host fitness. Quantitative PCR analysis of the bacterial population dynamics identified a remarkable interaction between the coexisting symbionts: Buchnera population was significantly suppressed in the presence of Rickettsia, particularly at the young adult stage, when the aphid most actively reproduces. On the basis of these results, we discussed the possible mechanisms that enable the prevalence of Rickettsia infection in natural host populations in spite of the negative fitness effects observed in the laboratory.     

EVOLUTION OF AN APHID-PARASITOID INTERACTION: VARIATION IN RESISTANCE TO PARASITISM AMONG APHID POPULATIONS SPECIALIZED ON DIFFERENT PLANTS

The evolution of associations between herbivorous insects and their parasitoids is likely to be influenced by the relationship between the herbivore and its host plants. If populations of specialized herbivorous insects are structured by their host plants such that populations on different hosts are genetically differentiated, then the traits affecting insect-parasitoid interactions may exhibit an associated structure. The pea aphid (Acyrthosiphon pisum) is a herbivorous insect species comprised of genetically distinct groups that are specialized on different host plants (Via 1991a, 1994). Here, we examine how the genetic differentiation of pea aphid populations on different host plants affects their interaction with a parasitoid wasp, Aphidius ervi. We performed four experiments. (1) By exposing pea aphids from both alfalfa and clover to parasitoids from both crops, we demonstrate that pea aphid populations that are specialized on alfalfa are successfully parasitized less often than are populations specialized on clover. This difference in parasitism rate does not depend upon whether the wasps were collected from alfalfa or clover fields. (2) When we controlled for potential differences in aphid and parasitoid behavior between the two host plants and ensured that aphids were attacked, we found that pea aphids from alfalfa were still parasitized less often than pea aphids from clover. Thus, the difference in parasitism rates is not due to behavior of either aphids or wasps, but appears to be a physiologically based difference in resistance to parasitism. (3) Replicates of pea aphid clones reared on their own host plant and on a common host plant, fava bean, exhibited the same pattern of resistance as above. Thus, there do not appear to be nutritional or secondary chemical effects on the level of physiological resistance in the aphids due to feeding on clover or alfalfa, and therefore the difference in resistance on the two crops appears to be genetically based. (4) We assayed for genetic variation in resistance among individual pea aphid clones collected from clover fields and found no detectable genetic variation for resistance to parasitism within two populations sampled from clover. This is in contrast to Henter and Via's (1995) report of abundant genetic variation in resistance to this parasitoid within a pea aphid population on alfalfa. Low levels of genetic variation may be one factor that constrains the evolution of resistance to parasitism in the populations of pea aphids from clover, leading them to remain more susceptible than populations of the same species from alfalfa.     

Variability in life history traits of the aphid,Acyrthosiphon pisum (Harris), from sexual and asexual populations

Many aphid species have shown remarkable adaptability by invading new habitats and agricultural crops, although they are parthenogenetic and might be expected to show limited genetic variation. To determine if the mode of reproduction limits the level of genetic variation in adaptively important traits, we assess variation in 15 life history traits of the pea aphid, Acyrhosiphon pisum (Harris), for five populations sampled along a north-south transect in central North America, and for three traits for three populations from eastern Australia. The traits are developmental times and rates as affected by temperature, body weights as affected by temperature, fecundity, measures of migratory tendency, and photoperiodic responses. The most southerly population from North America is shown to be obligately parthenogenetic, as are the Australian populations, and the four more northerly North American populations are facultatively parthenogenetic with the number of parthenogenetic generations per year increasing from north to south. The broad-sense heritabilities of life history traits varied from 0.36 to 0.71 for nine quantitive traits based on a comparison of within-and between-lineage variances. Using these traits, 7–13 distinct genotypes (i.e. clones) were identified among each of the 18 lines sampled from the North American populations, but the number did not differ significantly among populations. The level of genetic variation differed from trait to trait. For 4 of 12 quantitative traits, the level of variation in the obligately parthenogenetic population from North America was lowest, but significantly lower than all the sexual populations for only 1 trait. The obligately parthenogenetic population had the highest level of genetic variation for two traits, and had intermediate levels for the others. The most northerly population, which was sexual and had relatively few parthenogenetic generations each year, had the lowest level of variation for 5 of 12 traits and the highest level of variation for 2 traits. There was no decline in variability from north to south correlated with the increase in the annual number of parthenogenetic generations. The Australian populations showed no less variation than the North American populations for two of three traits, although the pea aphid was introduced to Australia only 5 years prior to the study, whereas the aphid has been in North America for at least 100 years. The mode of reproduction has not had a substantial impact on the level of genetic variation in life history traits of the pea aphid, but there are population-specific factors that effect the level of variation in certain traits.     

Patterns,causes and consequences of defensive microbiome dynamics across multiple scales

The microbiome can significantly impact host phenotypes and serve as an additional source of heritable genetic variation. While patterns across eukaryotes are consistent with a role for symbiotic microbes in host macroevolution, few studies have examined symbiont‐driven host evolution or the ecological implications of a dynamic microbiome across temporal, spatial or ecological scales. The pea aphid, Acyrthosiphon pisum, and its eight heritable bacterial endosymbionts have served as a model for studies on symbiosis and its potential contributions to host ecology and evolution. But we know little about the natural dynamics or ecological impacts of the heritable microbiome of this cosmopolitan insect pest. Here we report seasonal shifts in the frequencies of heritable defensive bacteria from natural pea aphid populations across two host races and geographic regions. Microbiome dynamics were consistent with symbiont responses to host‐level selection and findings from one population suggested symbiont‐driven adaptation to seasonally changing parasitoid pressures. Conversely, symbiont levels were negatively correlated with enemy‐driven mortality when measured across host races, suggesting important ecological impacts of host race microbiome divergence. Rapid drops in symbiont frequencies following seasonal peaks suggest microbiome instability in several populations, with potentially large costs of ‘superinfection’ under certain environmental conditions. In summary, the realization of several laboratory‐derived, a priori expectations suggests important natural impacts of defensive symbionts in host‐enemy eco‐evolutionary feedbacks. Yet negative findings and unanticipated correlations suggest complexities within this system may limit or obscure symbiont‐driven contemporary evolution, a finding of broad significance given the widespread nature of defensive microbes across plants and animals.     

Diversity and geographic variation of endosymbiotic bacteria in natural populations of the pea aphid (Acyrthosiphon pisum) in China

Bacterial symbionts in aphids are known to benefit the insect host and associated with aphid’s ecological adaptation. The pea aphid (Acyrthosiphon pisum), an important legume pest worldwide, carries at least eight endosymbionts, providing a model system to study insect–bacteria interactions. However, species diversity and geographic variations of endosymbionts are unknown in Chinese populations; therefore, we characterized symbiont communities and diversity of 27 pea aphid samples from 13 geographic populations of China. Via amplicon high-throughput sequencing and diagnostic PCR, we found that bacterial communities of Chinese populations were dominated by Proteobacteria and Firmicutes. Among eight known endosymbionts, five (Buchnera, Serratia, Hamiltonella, Regiella, and Rickettsia) were detected by both methods, with a specific geographical distribution. The obligate symbiont, Buchnera, was present in all aphid samples, while the four facultative symbionts showed a significant geographic variation. Each population was randomly infected with distinct endosymbionts, ranging from three to five species. Serratia and Rickettsia showed relatively higher abundance in central regions of China, Regiella was predominant in eastern and western China, whereas Hamiltonella showed an extremely low abundance and was absent in four populations. Samples grouped by altitudes showed a significant diversity difference, whereas there was no significant difference between red and green body colors. Bacterial community structures of the Chinese pea aphid populations were mainly influenced by environmental factors, other than body colors. These data can guide the development of potential biocontrol techniques against this aphid.     

Genome Sequence of the Pea Aphid Acyrthosiphon pisum

Aphids are important agricultural pests and also biological models for studies of insect-plant interactions, symbiosis, virus vectoring, and the developmental causes of extreme phenotypic plasticity. Here we present the 464 Mb draft genome assembly of the pea aphid Acyrthosiphon pisum. This first published whole genome sequence of a basal hemimetabolous insect provides an outgroup to the multiple published genomes of holometabolous insects. Pea aphids are host-plant specialists, they can reproduce both sexually and asexually, and they have coevolved with an obligate bacterial symbiont. Here we highlight findings from whole genome analysis that may be related to these unusual biological features. These findings include discovery of extensive gene duplication in more than 2000 gene families as well as loss of evolutionarily conserved genes. Gene family expansions relative to other published genomes include genes involved in chromatin modification, miRNA synthesis, and sugar transport. Gene losses include genes central to the IMD immune pathway, selenoprotein utilization, purine salvage, and the entire urea cycle. The pea aphid genome reveals that only a limited number of genes have been acquired from bacteria; thus the reduced gene count of Buchnera does not reflect gene transfer to the host genome. The inventory of metabolic genes in the pea aphid genome suggests that there is extensive metabolite exchange between the aphid and Buchnera, including sharing of amino acid biosynthesis between the aphid and Buchnera. The pea aphid genome provides a foundation for post-genomic studies of fundamental biological questions and applied agricultural problems.     

Predator avoidance behavior in the pea aphid: costs,frequency, and population consequences

Induced prey defenses can be costly. These costs have the potential to reduce prey survival or reproduction and, therefore, prey population growth. I estimated the potential for predators to suppress populations of pea aphids (Acyrthosiphon pisum) in alfalfa fields through the induction of pea aphid predator avoidance behavior. I quantified (1) the period of non-feeding activity that follows a disturbance event, (2) the effect of frequent disturbance on aphid reproduction, and (3) the frequency at which aphids are disturbed by predators. In combination, these three values predict that the disturbances induced by predators can substantially reduce aphid population growth. This result stems from the high frequency of predator-induced disturbance, and the observation that even brief disturbances reduce aphid reproduction. The potential for predators to suppress prey populations through induction of prey defenses may be strongest in systems where (1) predators frequently induce prey defensive responses, and (2) prey defenses incur acute survival or reproductive costs. Electronic supplementary material Supplementary material is available in the online version of this article at and is accessible for authorized users.     

Preceding crop affects soybean aphid abundance and predator–prey dynamics in soybean

Crop rotations alter the soil environment and physiology of the subsequent crop in ways that may affect the abundance of herbivores and their natural enemies. Soybean aphids are a consistent pest of soybean throughout North America, but little work has focused on how preceding crops may affect pest–predator dynamics. In a replicated experiment over three years, we examined how two preceding crops (spring wheat or an oat/pea mixture) affected seasonal soybean aphid pressure and the ratio of aphids to their predator community. Peak aphid populations were reduced by 40% and 75% in years 1 and 2 by planting spring wheat before soybeans (relative to the oat–pea mixture). Aphid densities were unaffected by preceding crop in the third year of study (aphids were at threshold in this year). Predators responded positively to aphid population increases and were unaffected by preceding crops. Additional research on how crop rotations can be used as a tool to manage soybean aphids warrants further attention.     

Variability in migratory tendency within and among natural populations of the pea aphid,Acyrthosiphon pisum

Summary The migratory tendencies of pea aphids were measured by determining the numbers of winged and non-winged offspring produced by parthenogenetic wingless females after a crowding test. Sources of variability in this measure were investigated. The migratory tendency of an individual clone was found to be stable. Spatial and temporal patterns in migratory tendency were found among nine natural populations. These patterns probably reflect differences in the frequencies of a large number of genetically distinct clones. Hypotheses based on the relative fitness of immigrant and resident clones and the heritability of migratory tendency are offered to account for these results. High migration rates may be required to account for genetic differentiation within and among some parthenogenetic populations of the pea aphid.     

The interplay between density- and trait-mediated effects in predator-prey interactions: a case study in aphid wing polymorphism

Natural enemies not only influence prey density but they can also cause the modification of traits in their victims. While such non-lethal effects can be very important for the dynamic and structure of prey populations, little is known about their interaction with the density-mediated effects of natural enemies. We investigated the relationship between predation rate, prey density and trait modification in two aphid-aphid predator interactions. Pea aphids (Acyrthosiphon pisum, Harris) have been shown to produce winged dispersal morphs in response to the presence of ladybirds or parasitoid natural enemies. This trait modification influences the ability of aphids to disperse and to colonise new habitats, and hence has a bearing on the population dynamics of the prey. In two experiments we examined wing induction in pea aphids as a function of the rate of predation when hoverfly larvae (Episyrphus balteatus) and lacewing larvae (Chrysoperla carnea) were allowed to forage in pea aphid colonies. Both hoverfly and lacewing larvae caused a significant increase in the percentage of winged morphs among offspring compared to control treatments, emphasising that wing induction in the presence of natural enemies is a general response in pea aphids. The percentage of winged offspring was, however, dependent on the rate of predation, with a small effect of predation on aphid wing induction at very high and very low predation rates, and a strong response of aphids at medium predation rates. Aphid wing induction was influenced by the interplay between predation rate and the resultant prey density. Our results suggests that density-mediated and trait-mediated effects of natural enemies are closely connected to each other and jointly determine the effect of natural enemies on prey population dynamics.     

Fitness effects of two facultative endosymbiotic bacteria on the pea aphid,Acyrthosiphon pisum,and the blue alfalfa aphid,A. kondoi

The effects of two bacterial endosymbionts, designated PASS and PAR, were evaluated on the pea aphid, Acyrthosiphon pisum (Harris) (Hemiptera:Aphididae), in which they occur facultatively, and on the blue alfalfa aphid, A. kondoi Shinji, in which these bacteria have not been found in natural populations. Subclones of pea aphids and blue alfalfa aphids, derived from parent aphid clones that did not contain PASS or PAR, were infected with one or both bacteria, generating PASS- and/or PAR-positive subclones with minimal genetic differences from the parent clones. Under laboratory conditions at 20 °C, PAR consistently reduced the fecundity (by between 19 and 60%) of subclones derived from three different parent pea aphid clones on bur clover, Medicago hispida Gaertn. PAR had intermediate effects on pea aphids reared on sweet pea, Lathyrus odoratus L., and had no significant effect on pea aphids on alfalfa, Medicago sativa L. The effect of PASS was either neutral or negative, depending on parent clone as well as host plant. Also at 20 °C, PASS reduced fecundity (70–77%) and longevity (40–48%), and increased the age of first reproduction (by up to 1.5 days) of blue alfalfa aphid reared on alfalfa and clover. PAR had a less dramatic effect (e.g., 30–39% reduction in fecundity) on these traits of blue alfalfa aphid. In contrast, PAR and PASS increased the fitness of pea aphid subclones of one parent clone reared for three generations at 25 °C on each of the three test plants. Without facultative bacteria, fecundity of the parent clone was reduced to a mean total of < 6 offspring per adult at this elevated temperature, but with PASS or PAR, mean total fecundity of its subclones was > 35. However, this ameliorative effect of facultative bacteria at 25 °C was not found for two other sets of parent clones and their derived subclones. Alate production in pea aphids was significantly increased in large populations of two PASS- and PAR-positive subclones relative to their parent clones. Attempts to transmit PASS or PAR horizontally, i.e., from aphid to aphid via feeding on host plants (bur clover), were unsuccessful.     

Influence of Experience on the Response of Bathyplectes curculionis (Hymenoptera: Ichneumonidae), a Nonaphidophagous Parasitoid, to Aphid Odor

Bathyplectes curculionis (Thomson) is an introduced natural enemy of the alfalfa weevil in North America. The wasp requires carbohydrate foods as an adult. Adult wasps have increased longevity and fecundity when provided access to pea aphid, Acyrthosiphon pisum (Harris), honeydew in the laboratory, and adults respond positively to the presence of pea aphids in alfalfa fields. However, it is unknown how these wasps find aphid honeydew in the field. In a series of Y-tube olfactometer experiments, we evaluated the response of naïve and experienced adult female B. curculionis to odors from pea aphids, alfalfa, and pea aphids on alfalfa. Naïve adult females did not respond positively to pea aphid odor even when hungry. But adult females were able to learn aphid odor, and the mechanism of learning appears to be associative rather than by sensitization. Naïve females also showed no preference for alfalfa odor but learned alfalfa odor through sensitization. The wasps did not distinguish between alfalfa with aphids and alfalfa without aphids, even after exposure to aphids or alfalfa with aphids. However, they preferred pea aphid odor to alfalfa odor after a feeding experience in the presence of pea aphid odors. But after exposure to mixed odors of aphids and alfalfa while feeding, B. curculionis females preferred the odor of alfalfa to the odor of pea aphids. These results suggest that alfalfa odors mask or override aphid odors when aphids are associated with alfalfa (as happens naturally), thus interfering with the wasp's ability to respond to learned aphid odors. Therefore, although the wasps are capable of learning to find pea aphids and their honeydew in a simplified laboratory setting, it appears unlikely that they do so in the field.