Reproductive mode and population genetic structure of the cereal aphid Sitobion avenae studied using phenotypic and microsatellite markers

As French populations of the aphid Sitobion avenae exhibit a range of reproductive modes, this species provides a good opportunity for studying the evolution of breeding system variation. The present analysis combined ecological and genetic investigations into the spatial distribution of variation in reproductive mode. Reproductive mode was characterized in 277 lineages of S. avenae from France, and these aphids were scored for five microsatellite loci. The analyses revealed strong geographical partitioning of breeding systems, with obligate asexuals mostly restricted to the south of France, while lineages producing sexual forms were more common in the north. Contrary to what might be anticipated for organisms with frequent parthenogenesis, there was substantial genic and genotypic diversity, even in the obligately asexual lineages. More than 120 different genotypes were detected among the 277 aphid lineages, with an average of 5.9 alleles per locus (range four to 16) and heterozygosity of 56.7%. As with previous studies of allozyme variation in aphids, most loci showed heterozygote deficits, and disequilibrium was common among allelic variants at different loci, even after removal of replicate copies of genotypes that might have been derived through clonal reproduction. Our results suggest that selection is important in structuring reproductive systems and genetic variation in French S. avenae. Canonical correspondence analysis was employed to examine the associations between genotypic and phenotypic variables, enabling the identification of alleles correlated with life-history traits.     

Production of sexual morphs by the monoecious cereal aphid Sitobion avenae

The effects of photoperiod and temperature on the production of sexual forms by two clones of Sitobion avenae, the grain aphid, were examined. One clone did not produce sexual forms, whereas the other did under conditions of short light (<14 h) and low temperature (15°C). Temperature and photoperiod interacted to some extent both in the production of oviparae and of males. Even when the sexual forms were produced there was always a proportion of virginoparae.

---

Production de sexués par Sitobion avenae, puceron monoécique

Résumé Un clone de Sitobion avenae a produit sans difficulté jusqu'à 7 générations de sexués en réaction à des photopériodes courtes (<14 h) et à de faibles températures (15°C) tandis qu'un autre clone n'en produit aucune.La proportion de sexués différait suivant les parents. La production de mâles avait une nette tendance à apparaître lors des reproduction les plus tardives. Dans les générations tardives avec jours courts, les vivipares (virginopares et gynopares) avaient eu tendance à être produits à la fin de la période de reproduction.Les gynopares (c'est à dire les parents d'ovipares) de S. avenae étaient surtout aptères, mais comprenaient beaucoup plus d'ailés que les virginopares obtenus dans les mêmes conditions. Un vivipare était induit comme gynopare (ou ses embryons étaient déterminés comme ovipares) avant la naissance, mais cette détermination pouvait apparemment encore être inversée en soumettant l'insecte à de longues photopériodes et à de hautes températures jusqu'à deux jours après la naissance.Aucun S. avenae ovipare n'a été produit jusqu'à la troisième génération. Aucun ovipare n'a été produit avec des photopériodes supérieures à 13 H 30 à 10°C, 13 H à 15°C et 8 H à 20°C. La proportion d'individus produisant des ovipares à 15°C a été plus faible qu'à 10°C pour toutes les photopériodes, et à cette dernière température beaucoup plus de vivipares étaient gynopares que virginopares.Les basses températures ont été vraisemblablement le facteur dominant de stimulation de la production de mâles de S. avenae, mais cependant il semble qu'un plus grand nombre de mâles a été produit aux températures et photopériodes intermédiaires qu'aux extrêmes.La capture de mâles ailés de S. avenae dans des pièges à succion a été généralement limitée à Octobre-soit à peu prés le moment prévu par les expériences de laboratoire. Des mâles de S. avenae sont aussi capturés fréquemment et été, ce qui peut être lié à des hivers précédents doux.

     

Influence of the hyperparasitoid Dendrocerus carpenteri on the reproduction of the grain aphid Sitobion avenae

1.Alate S. avenae (F.) reproduced earlier and produced more offspring in the vicinity of Dendrocerus carpenteri (Curtis) females than control aphids without neighbouring hyperparasitoids.
2. This effect was evident only during the first 6 days of the aphid's reproduction period and did not affect the physiological condition of the aphids or their offspring.
3. Virgin hyperparasitoid females had a stronger influence on the reproduction rate of the aphids than did mated females, probably due to an unidentified emitted volatile sex pheromone.     

Cold hardiness and overwintering of the grain aphid Sitobion avenae

ABSTRACT.

• 1 Cold hardiness as measured by supercooling ability in the active stages of the grain aphid Sitobion avenae (F.) decreased progressively with maturation.
• 2 Aphids showed no acclimation response when maintained at low temperatures.
• 3 Starvation did not improve supercooling ability.
• 4 In a single exposure, surface moisture caused inoculation above the inherent supercooling point in a small proportion of a population.
• 5 Field populations show a seasonal change in supercooling ability, which is at a maximum in summer and a minimum in late winter.
• 6 It is concluded that the act of feeding on healthy plant tissue may confer extensive supercooling ability.

     

麦长管蚜脱巴克纳氏共生菌的分子验证

蚜虫脱共生效果的鉴定对蚜虫-巴克纳氏菌共生体系的研究至关重要.采用光学显微镜观察及特异性PCR扩增技术,对麦长管蚜(Sitobion aoenae)脱巴克纳氏共生菌的效果进行了研究.结果表明:用利福平处理5 d和10 d后的麦长管蚜,PCR检测发现有巴克纳氏菌(Buchnera)特异性扩增条带,说明共生菌仍然存在;在利福平处理 15 d后,PCR检测没有发现特异性扩增条带,说明麦长管蚜胞内共生细菌的核酸已经被降解;光学显微镜观察与PCR检测结果相一致.     

Fitness traits and underlying genetic variation related to host plant specialization in the aphid Sitobion avenae

Sitobion avenae （E） is an important cereal pest worldwide that can survive on various plants in the Poaceae, but divergent selection on different host plants shouldpromote the evolution of specialized genotypes or host races. In order to evaluate their resource use strategies, clones of S. avenae were collected from oat and barley. Host-transfer experiments for these clones were conducted in the laboratory to compare their fitness traits. Our results demonstrated that barley clones had significantly lower fecundityand tended to have longer developmental times when transferred from barley to oat. However, oat clones developed faster after they were transferred to barley. Clones fromoat and barley had diverged to a certain extent in terms of fecundity and developmental time of the nymphs. The separation of barley clones and oat clones of S. avenae was alsoevident in a principal component analysis. Barley clones tended to have higher broad-sense heritabilities for fitness traits than oat clones, indicating the genetic basis of differentiationbetween them. Barley clones showed significantly higher extent of specialization compared to oat clones from two measures of specialization （i.e., Xsp and Ysp）. Therefore, barleyclones were specialized to a certain extent, but oat clones appeared to be generalized. The fitness of S. avenae clones tended to increase with higher extent of specialization. Theevolution toward ecological specialization in S. avenae clones, as well as the underlying genetic basis, was discussed.     

Seasonal and annual genotypic variation and the effect of climate on population genetic structure of the cereal aphid Sitobion avenae in northern France

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.     

Genetic structure and clonal diversity of an introduced pest in Chile, the cereal aphid Sitobion avenae

In Chile, the aphid Sitobion avenae is of recent introduction, lives on cultivated and wild Poaceae, and is thought to reproduce by permanent parthenogenesis. In order to study the genetic variability and population structure of this species, five microsatellite loci were typed from individual aphids collected from different cultivated and wild host plants, from different geographical zones, and years. Chilean populations showed a high degree of heterozygosity and a low genetic variability across regions and years, with four predominant genotypes representing nearly 90% of the sample. This pattern of low clonal diversity and high heterozygosity was interpreted as the result of recent founder events from a few asexually reproducing genotypes. Most geographical and temporal variation observed in the genetic composition resulted from fluctuations of a few predominant clones. In addition, comparisons of the genotypes found in Chile with those described in earlier surveys of S. avenae populations in Western Europe led us to identify 'superclones' with large geographical distribution and high ecological success, and to make a preliminary exploration of the putative origin(s) of S. avenae individuals introduced to Chile.     

Antimetabolic effect of phytohemagglutinin to the grain aphid Sitobion avenae fabricius

The insecticidal activity of plant lectins against a wide range of insect species have been intensively studied. Understanding the mechanism of the toxicity of lectins is one of the studied aspects. In the present research, the first step was determine the effect of phytohemagglutinin (PHA) on the development, fecundity and mortality of grain aphid. Next, the effect of PHA lectin on the activity of such enzymes as: α- and β-glucosidases, alkaline (AkP) and acid (AcP) phosphatases, aminopeptidase N and cathepsin L involved in the metabolism of sugar, phosphorus and proteins of an adult apterae aphids was investigated. The PHA lectin added into the liquid diet increased the pre-reproductive period, mortality of Sitobion avenae, the time of generation development and decreased its fecundity and the intrinsic rate of natural increase. In addition, activity of α-glucosidase, alkaline phosphatase and aminopeptidase N of adult apterae exposed to PHA were reduced. The results indicate that the insecticidal activity of PHA on S. avenae may involve changes in activity of the enzymes in the midgut and it may be part of its toxicity.     

Host selection by winged summer females of the aphid Sitobion avenae

A total of 55 parthenogenetic lineages of the grain aphid, Sitobion avenae F. were established from single clones collected from winter wheat (agricultural host) and cocksfoot (natural host) at various locations in southern Britain. RAPD-PCR profiles indicated that these lineages consisted of at least 15 genetically distinct clones. Twenty winged individuals (alatae) of known weight were taken from each lineage and presented with a choice of wheat and cocksfoot hosts (with a total leaf area each of 2 cm²) held in petri dishes (laboratory experiments) and flowerpots (field experiments). In both experimental designs host preferences were determined by a ranking of a proportion of counts (limited to -1 +1) of the progeny produced on each host after 5 days. Overall, alatae tended to prefer the agricultural host. However, alatae from individual clones found exclusively on wheat generally had a higher preference for wheat than alatae from individual clones found exclusively on cocksfoot. Wheat-derived lineages (aphid genotypes that were collected on wheat but also present on cocksfoot) showed a significantly greater preference for the agricultural host than the cocksfoot-derived lineages. Individuals from a wheat-derived lineage had significantly higher observed and potential progeny production on wheat than they did on cocksfoot, while individuals from a cocksfoot-derived lineage had significantly higher potential progeny but lower mean progeny weights on wheat. In a second stage, reciprocal host transfer experiments were carried out in the laboratory, i.e. lineages collected from the agricultural host were reared for several generations on the natural host and vice versa prior to being tested for host preference. The preference of the lineages for their host of origin significantly decreased in this second trial, reversing the overall preference trends, while there was little evidence for between-lineage variation in this change in preference. In summary these results indicate weak genotypic but strong environmental influences on alate host preference in S. avenae. This host plant conditioning effect may serve to promote host-based genetic structuring observed in southern British populations of S. avenae.     

Toxic and deterrent effects of phytohemagglutinin on the grain aphid Sitobion avenae

The toxicity and deterrent effects of phytoheamagglutinin (Phaseolus vulgaris agglutinin, PHA) to the grain aphid (Sitobion avenae F.) was investigated in the laboratory by use of liquid diets or gels containing various PHA concentrations. The addition of PHA to the liquid diet increased the aphid pre-reproductive period, mortality, and generation time and decreased aphid fecundity and intrinsic rate of natural increase. Aphids fed on sucrose-agarose gels with higher concentrations of PHA exhibited no phloem-feeding behavior. The number of gel penetrations was reduced and duration of the pathway phase was increased as PHA concentration increased. These results indicate that PHA is detrimental to S. avenae and that the effect of PHA is at least partially explained by suppression of feeding behaviour. PHA could be useful for managing S. avenae.     

Migration and genetic structure of the grain aphid (Sitobion avenae) in Britain related to climate and clonal fluctuation as revealed using microsatellites

Genetic structuring of populations reflects the interaction of genetic drift, mutation, migration and selection, with influences from life history. Aphids are interesting in this regard as they have the potential for unusually high levels of dispersal and natural selection, which typically counter each other. In the present study, winged grain aphids Sitobion avenae (F.) were collected in four 12.2-m high suction traps along a north-south transect in Britain in order to eliminate sampling bias from plant hosts (cereals and grasses; Poaceae), it being known that these insects show host adaptation demonstrable using molecular markers. Samples were analysed at four polymorphic microsatellite loci over two consecutive years. Population allele frequencies were similar nationally during the two years, although clonal diversity varied greatly between sites and years. In the first sampling year following a harsh winter, diversity was found to display a latitudinal clinal trend: the proportion of unique clones (genotypes) increased with latitude. However, this pattern was less apparent the following year, after a milder winter. Nonetheless, overall FST analysis showed that there was little spatial genetic structuring in either sampling year. These data support the view that the insect is highly migratory and also support a theoretical model and previous data suggesting that the reproductive mode is clinal in S. avenae. This appears to be because natural selection (reduced reproductive success of asexual genotypes under cold conditions) is sufficiently powerful to overcome the homogenizing effects of strong migration. There was no clear evidence for isolation by distance for the genetic data obtained. The data are compared with similar data from other aphid species and other insects. Only by the collection of such data sets can an accurate picture be built up relating genetic variability to flight behaviour, including migratory ambit in this group of insects since, due to their small size and rapid dilution in the air, other marking approaches are impracticable over large geographical distances.     

Insight into watery saliva proteomes of the grain aphid,Sitobion avenae

The grain aphid, Sitobion avenae, is an economically important cereal pest worldwide. Aphid saliva plays an essential role in the interaction between aphids and their host plants. However, limited information is available regarding the proteins found in the saliva of S. avenae. Here, the watery saliva proteins from S. avenae were collected in an artificial diet and identified using a liquid chromatography–mass spectrometry/mass spectrometry analysis. A total of 114 proteins were identified in S. avenae saliva, including several enzymes, binding proteins, and putative effectors, as well as other proteins with unknown functions. In comparison with salivary proteins from nine other aphid species, the most striking feature of the salivary protein from S. avenae was the different patterns of protein functions. Several orthologous proteins secreted by other aphid species such as glucose dehydrogenase, elongation factors, and effector C002 were also detected in S. avenae saliva and speculated to play a significant role in aphid–plant interactions. These results provide further insight into the molecular basis between aphids and cereal plant interactions.     

Life-cycle variation in the aphid Sitobion avenae: costs and benefits of male production

Abstract 1. Patterns of male production and life-cycle variation were investigated in the aphid Sitobion avenae . Seventy-seven field-collected clones were subjected to a 14 °C short day-length regime to assess their reproductive modes, and three clones were used to study life-cycle inheritance. A further analysis assessed the cost of male production.
2. In comparison with those from East Anglia, there were more holocyclic and intermediate clones found in Scottish populations, and they produced significantly more mating females. In total, 44% of clones were androcyclic.
3. The inheritance of life cycle showed a greater level of complexity than could be achieved by previously suggested monohybrid inheritance mechanisms.
4. Holocyclic and intermediate clones produced a higher proportion of males than did androcyclic clones. Inter-clonal differences were reflected in the pattern of male production in the reproductive sequence.
5. A significant cost was associated with male production in terms of a reduction in both fecundity and total offspring biomass.
6. Winged females rarely gave birth to males but the pattern of mating female production differed between holocyclic and intermediate clones.
7. Patterns of male and mating female production by the different types of clone may be related to different advantages and disadvantages of dispersal and inbreeding.
8. Recent models of aphid overwintering could be enhanced by consideration of issues raised in this study, such as the cost of male production, the inheritance of life cycle, and the patterns of sexual morph production.     

The spatial and temporal distribution of the grain aphid Sitobion avenae in winter wheat

The spatial and temporal distribution of the grain aphid Sitobion avenae F. (Homoptera: Aphididae) was studied within a field of winter wheat during the summer of 1996. Sampling was done using four nested grids comprising 133 locations. Analysis by Taylor's power law gave results typical for insect populations. Analysis by SADIE (Spatial Analysis by Distance Indices) showed spatial pattern due to edge effects and sampling scale, and positive but mild spatial association, although spatial patterns were ephemeral. Reasons for these findings and the implications for integrated crop management are discussed.     

Predation of the cereal aphid Sitobion avenae by polyphagous predators on the ground

Abstract. 1. Polyphagous predator densities were manipulated in a wheat crop using polythene exclusion barriers.
2. The rates at which aphids fell to the ground and subsequently climbed and returned to the crop canopy were measured.
3. Peak aphid density was highest when polyphagous predator density was lowest.
4. Similar rates of aphid fall-off were measured in each plot, but aphid climbing rate was highest when predator densities were lowest.
5. It was concluded that ground-zone predators reduced the rate at which aphids return to the crop canopy.     

Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenae

Polyacrylamide gel electrophoresis was used to monitor levels of parasitism in field populations of the cereal aphid, Sitobion avenae (F.) (Hemiptera: Aphididae). Electrophoretic keys previously prepared from laboratory-reared parasitoids were used to identify parasitoids within field-collected aphids. Using this approach, the primary parasitoids Aphidius rhopalosiphi De Stefani Perez, Aphidius ervi (Haliday), Aphidius picipes (Nees), Praon volucre Haliday, Ephedrus plagiator Nees and Aphelinus abdominalis Dalman were detected. Some unidentified banding patterns were also obtained, most of which were probably attributable to the presence of hyperparasitoids. Electrophoresis was compared with the more conventional sampling techniques of live-rearing and mummy counts as a means of estimating percentage parasitism. Electrophoresis was found to be a much quicker method than live-rearing and gave similar results for both levels of parasitism and parasitoid species composition, whereas mummy counts tended to give lower estimates than the other two methods.

---

Résumé L'électrophorèse sur gel de polyacrylamide a servi à déterminer l'importance du parasitisme de populations naturelles de S. avenae F. Des clés électrophorétiques, préparées à partir de parasitoïdes élevés au laboratoire, ont été utilisées pour identifier les parasitoïdes provenant des pucerons récoltés dans la nature. Ainsi ont été décelés les parasites primaires: Aphidius rhopalosiphi De Stefani Perez, A. ervi Haliday, A. picipes Nees, Praon volucre Haliday, Ephedrus plagiator Nees et Aphelinus abdominalis Dalman. Quelques bandes non-identifiées devraient être attribuées à des hyperparasitoïdes. L'électrophorèse a été comparée aux techniques d'échantillonnage plus conventionnelles de décompte des momies et d'élevage des individus vivants utilisées pour estimer le taux de parasitisme. L'électrophorèse et les méthodes d'élevage donnent généralement des résultats semblables pour les 2 niveaux de parasitisme et la composition en espèces de parasitoïdes, tandis que le décompte des momies tend à donner des résultats inférieurs.

     

Incidence of parasitism by Aphidius rhopalosiphi in colour forms of the aphid Sitobion avenae

Aphidius rhopalosiphi parasitises green colour forms of Sitobion avenae more frequently than brown forms. The handling time is longer for brown than for green nymphs, even when the two forms are members of the same clone. Parasite development lasts longer in brown forms than in green forms, and mortality is higher.

---

Résumé A. rhopalosiphi a parasité les stades jeunes de S. avenae avec plus de succès que les stades âgés, et les types verts plus fréquemment que les bruns. Dans tous les cas, la mortalité était élevée; significativement plus de pucerons du premier et du second stade ont été tués par l'attaque du parasite que ceux des 3è et 4è stades. La fréquence de pucerons bruns formant des momies a augmenté avec le nombre de pipûres, de 0,1 pour une piqûre à 0,4 pour 8 piqûres. Lorsqu'il n'y a qu'une piqûre, le nombre d'oeufs émis est le même pour les deux types. A 20–22 °C, le développement du parasite dure jusqu'à 9 jours dans les pucerons verts et 12 jours dans les bruns. Lorsqu'il y a choix, les parasites préfèrent les verts aux bruns (Même quand ils sont du même clone) et les bruns clair aux bruns sombres. Les verts ont besoin de moins de rencontres que les bruns pour être piqués, mais pour une souche de parasites recueillie depuis peu, la différence était faible, pourtant cette nouvelle souche ne parasitait pas les pucerons bruns avec plus de succès que l'ancienne souche.