Longitudinal clines in the frequency distribution of 'super-clones' in an aphid crop pest.

Parthenogenesis is the main mode of reproduction of aphids. Their populations are therefore composed of clones whose frequency distribution varies in space and time. Previous population genetic studies on aphids have highlighted the existence of highly abundant clones ('super-clones'), distributed over large geographic areas and persisting over time. Whether the abundance of 'super-clones' results from their ecological success or from stochastic forces, such as drift and migration, is an open question. Here, we looked for the existence of clines in clonal frequency along a climatic gradient in the cereal aphid Rhopalosiphum padi (Linnaeus, 1758) and examined the possible influence of geographical distance and environmental variables in the buildup and maintenance of such clonal clines. We investigated the spatial distribution of the commonest genotypes of R. padi by sampling populations along an east-west transect in maize fields in the northern half of France in both spring and late summer. Individual aphids were genotyped at several polymorphic loci, allowing the assessment of frequency distributions of multilocus genotypes (MLGs) across the cropping season. We found several MLGs showing longitudinal clines in their frequency distribution in both spring and summer. In particular, two dominant asexual genotypes of R. padi showed inverted geographical clines, which could suggest divergent adaptations to environmental conditions. We concluded that while the distribution of some 'super-clones' of R. padi seems most likely driven by the action of migration and genetic drift, selection could be also involved in the establishment of longitudinal clines of others.

The genetics of obligate parthenogenesis in an aphid species and its consequences for the maintenance of alternative reproductive modes.

Although loss of sex is widespread among metazoans, the genetic mechanisms underlying the transition to asexuality are poorly understood. Aphids are good models to address this issue because they frequently show reproductive-mode variation at the species level, involving cyclical parthenogens (CP) that reproduce sexually once a year and obligate parthenogens (OP) that reproduce asexually all year round. Here, we explore the genetic basis of OP in the cereal aphid Sitobion avenae by crossing several genotypes with contrasting reproductive modes and then characterising the reproductive phenotypes of F1 and F2 offspring. The analysis of phenotypic variation in F1 and F2 progenies suggests that at least two autosomal loci control OP in S. avenae. First, the transition to asexuality seems to depend on a single recessive locus, because the offspring from self-crossed cyclical parthenogenetic genotypes contain either 0 or 25% OP. Second, as we observed OP in the F1 progenies from crosses between CP and OP, and some CP in the offspring from outcrossed OP, a dominant 'suppressor' gene may also be involved, being inactive when in a recessive homozygous state in CP; this is the most parsimonious explanation for these results. This oligogenic inheritance of OP in S. avenae appears to be an efficient genetic system to generate new OP genotypes continually. It also allows asexuality-inducing alleles to be protected locally during harsh winters when extreme frost kills most OP, and then to spread very quickly after winter.

Climate and agricultural context shape reproductive mode variation in an aphid crop pest.

In aphids, reproductive mode is generally assumed to be selected for by winter climate. Sexual lineages produce frost-resistant eggs, conferring an advantage in regions with cold winters, while asexual lineages predominate in regions with mild winters. However, habitat and resource heterogeneities are known to exert a strong influence on sex maintenance and might modulate the effect of climate on aphid reproductive strategies. We carried out a hierarchical sampling in northern France to investigate whether reproductive mode variation of the aphid Rhopalosiphum padi is driven by winter climate conditions, by habitat and resource heterogeneities represented by a range of host plants or by both factors. We confirmed the coexistence in R. padi populations of two genetic clusters associated with distinct reproductive strategies. Asexual lineages predominated, whatever the surveyed year and location. However, we detected a between-year variation in the local contribution of both clusters, presumably associated with preceding winter severity. No evidence for host-driven niche differentiation was found in the field on six Poaceae among sexual and asexual lineages. Two dominant multilocus genotypes ( approximately 70% of the sample), having persisted over a 10-year period, were equally abundant on different plant species and locations, indicating their large ecological tolerance. Our results fit theoretical predictions of the influence of winter climate on the balance between sexual and asexual lineages. They also highlight the importance of current agricultural practices which seem to favour a small number of asexual generalist genotypes and their migration across large areas of monotonous environments.

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.

Predominance of sexual reproduction in Romanian populations of the aphid Sitobion avenae inferred from phenotypic and genetic structure.

Models of coexistence of sexual and asexual lineages in aphids assume that obligate parthenogenetic lineages predominate in areas with mild winter climate because of their high reproductive output, while sexual lineages predominate in areas with severe winter because they produce eggs resistant to frost. To validate this hypothesis in natural conditions, the reproductive mode of populations of the aphid Sitobion avenae was assessed in two very contrasting climatic situations, Romania (severe winter) and Western France (mild winter). To achieve this, reproductive modes were inferred from both (1) the population composition in sexual and asexual forms in autumn, and (2) the genetic structure of Romanian and French populations of S. avenae using microsatellite markers. Romanian populations encompassed a high proportion of sexual forms and were characterised by a very high genotypic diversity and low linkage disequilibrium. In constrast, the French population showed frequent linkage disequilibria, low genetic diversity, and high level of clonal amplification with two asexual genotypes representing over 60% of the sample. In agreement with the model's predictions, these results clearly indicate that sexual reproduction in S. avenae is predominant under the continental climate of Romania, while asexual lineages prevail under the oceanic climate of Western France.

Aphid Abundance on Cereals in Autumn Predicts Yield Losses Caused by Barley yellow dwarf virus.

ABSTRACT Barley yellow dwarf virus (BYDV) damage to winter cereals and population dynamics of the aphid Rhopalosiphum padi during fall were monitored in fields during 10 years at various locations in the northern half of France. Logistic regression was used to examine whether a simple risk probability algorithm based only on the autumnal population dynamics of R. padi can accurately predict yield losses caused by BYDV and, therefore, the need for insecticide treatment. Results showed that the area under the curve of the percentage of plants infested by R. padi during autumn was highly significantly related to BYDV yield losses. Then, a cost/benefit analysis was performed to estimate the optimal decision threshold resulting in the lowest annual average costs of BYDV damage and control. A "model use" strategy allowed a reduction in the annual average costs of BYDV disease and control of up to 36% when compared with a "prophylactic spraying" strategy. The optimal decision threshold was highly sensitive to variation in disease prevalence. This property was used to propose an easy way to adapt the model to any production situation through the determination of the most accurate decision threshold.

Two-dimensional electrophoresis of proteins discriminates aphid clones of Sitobion avenae differing in BYDV-PAV transmission.

Aset of 39 F1 Sitobion avenae clones was obtained by selfing a poorly efficient BYDV-PAV vector clone. These clones were genetically typed by 11 microsatellite loci, and tested for BYDV-PAV4 transmission to barley. The 39 clones displayed a continuum in transmission percentages, from 0% to 88% with a significant clone effect. From this set, two highly efficient (HEV) and two poorly efficient (PEV) vectoring clones were more precisely characterized for transmission of two other PAV isolates. The molecular bases of the lower transmissibility of BYDV-PAV4 by PEV clones and of the aphid vectoring properties were investigated respectively by comparing the sequences corresponding to structural proteins (CP and RTD) of BYDV, and by using proteomic analysis of aphids in two dimensional electrophoresis (2-DE) with immobilized pH gradients (IPG) after an improved protein extraction. Four residues specific to BYDV-PAV4 located in the CP sequence (A(24) and L(130)) or in the RTD region (M(334) and S(456)) could be responsible for the lower transmissibility of this isolate by PEV clones. Among a total of 2150 well-resoluted spots scored on S. avenae proteinic pattern, only twelve proteins were qualitatively or quantitatively different between clones. Four out of them discriminated HEV and PEV groups.

Evidence for predominant clones in a cyclically parthenogenetic organism provided by combined demographic and genetic analyses.

Aphids are particularly interesting models in the study of genetic and demographic components of plant adaptation because of their breeding system which combines parthenogenesis and sexual reproduction (i.e. cyclical parthenogenesis), and the frequent emergence of host-adapted races reported in this group. In this paper, patterns of host adaptation were assessed on local populations of the aphid Sitobion avenae by following their demographic and genetic structure in a maize field for two consecutive years. The existence of putative generalist (polyphagous) or specialized (host-adapted) genotypes was also investigated by comparing the genotypic distribution of this aphid on maize and other cultivated host plants, using five microsatellite loci. Although population dynamics revealed strong variation in aphid abundance during the colonization period on maize, two genotypes identified at seven additional microsatellite loci were predominant and exhibited stable frequencies over cropping season and between years. Based on present and earlier studies, these two prevalent genotypes were shown to survive on different host plants other than maize, to colonize large geographical zones and to persist parthenogenetically for several years. All these data strongly suggest that these two genotypes are asexual generalist clones that could have been favoured by agricultural practices encountered in western Europe. Besides these two clones, a continual replacement of rare genotypes was observed on maize in both years. Hypotheses involving selection via aphid-plant interactions and natural enemies were proposed for explaining the disappearance of these genotypes on maize.

Analyzing and Modeling Temporal Disease Progress of Barley yellow dwarf virus Serotypes in Barley Fields.

ABSTRACT Population dynamics of Padi avenae (PAV), Macrosiphum avenae (MAV), and Rhopalosiphum padi (RPV) virus serotypes of Barley yellow dwarf virus (BYDV) and of their main aphid vectors were studied in winter barley (Hordeum vulgare) fields for three successive years in western France. An epidemiological model of the spread of viruses in the field was developed based on vector populations as forcing variables and the population dynamics of each virus serotype. This model accurately simulated the kinetics of the epidemic for PAV serotypes, which are the most common ones. For RPV and to some extent for MAV, the results were less satisfactory. The occurrence and spread of PAV and MAV serotypes in the field was clearly and easily related to that of their main vector species. Conversely, the spread of RPV serotypes showed no consistent relationships with the dynamics of their vectors. Incidence of PAV in 1989 to 1990 and 1990 to 1991 showed a bimodal distribution, with maximums in fall (December) and spring (May) that were linked to fall infestations by R. padi and spring infestations by three (R. padi, Sitobion avenae, and Metopolophium dirhodum) or two (S. avenae and M. dirhodum) aphid species. In 1991 to 1992, the PAV infection curve was monomodal and mainly due to a primary spread of the virus by very large populations of alate R. padi. MAV incidence was low in fall and winter and reached a maximum in spring 1990 and 1991 related to the occurrence of S. avenae and M. dirhodum. RPV incidence was low every year, despite the abundance of its vector, R. padi. Mixed infections were more frequent than expected by chance and were assumed to be partly related to heterologous encapsidation. The occurrence of each serotype is discussed in relation to the time of crop infection and possible damage.

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.