Spatial and temporal genetic variability in French populations of the peach-potato aphid,Myzus persicae

The peach-potato aphid, Myzus persicae (Sulzer), has a complex reproductive mode in which some lineages reproduce by continuous parthenogenesis, whereas others reproduce sexually once a year. The climate is thought to act directly on the reproductive mode, because sexual eggs are the only form that can resist frost in cold regions. Sexual reproduction necessitates an obligatory host alternation that may result in long-distance dispersal. Here, we examined the genetic variability at seven microsatellite loci of populations of M. persicae in France, where both reproductive modes occur. We provide clear genetic evidence that the breeding system affects genotypic variability, as cyclically parthenogenetic aphids are far more variable than their obligately parthenogenetic counterparts. A temporal decrease in genetic variability and a temporal genetic differentiation effect suggest the existence of selective factors that play an important role in shaping the genetic structure of M. persicae populations. Lastly, differences in the population structure between reproductive modes suggest that the migration associated with the change of host during sexual reproduction lowers the level of population differentiation.     

Incidence of insecticide resistance alleles in sexually-reproducing populations of the peach-potato aphid Myzus persicae (Hemiptera: Aphididae) from southern France

Intensive chemical treatments have led to the development of a number of insecticide resistance mechanisms in the peach-potato aphid Myzus persicae (Sulzer). Some of these mechanisms are known to be associated with negative pleiotropic effects (resistance costs). Molecular and biochemical methods were used to determine the genotypes or phenotypes associated with four insecticide resistance mechanisms in single aphids from sexually-reproducing populations in southern France. The mechanisms considered were E4 and FE4 carboxylesterase overproduction, modified acetycholinesterase, and kdr and rdl resistance-associated mutations. A new method for determining individual kdr genotypes is presented. Almost all resistant individuals overproduced FE4 carboxylesterase, whereas modified acetylcholinesterase was rare. Both the kdr and rdl resistance mutations were present at high frequencies in French sexually-reproducing populations. The frequencies of insecticide resistance genes were compared before and after sexual reproduction in one peach orchard at Avignon to evaluate the potential impact of selection on the persistence of resistance alleles in the over-wintering phase. The frequencies of the kdr and rdl mutations varied significantly between autumn and spring sampling periods. The frequency of the kdr mutation increased, probably due to pyrethroid treatments at the end of the winter. Conversely, the frequency of the rdl mutation decreased significantly during winter, probably because of a fitness cost associated with this mutation.     

Antibiotic resistance in potato cultivars to the aphid Myzus persicae

Commercially-grown potato cultivars were assessed for antibiotic resistance to Myzus persicae in a culture room at 19°C with a 2°C range and a 16 h photoperiod. The resistant rankings obtained were consistent for the following aphid metrics: maturation time, teneral adult weight, embryo complement and the production of nymphs. Intrinsic rates of increase (r_m) correlated with the above parameters of aphid growth and reproduction but this was not always the case for nymphal survival rate. The cultivars Ulster Tarn, Record and Maris Piper were relatively resistant to M. persicae and cultivars Desirée and King Edward were the most susceptible. When the aphid clone or the culture plants were changed there was no significant effect on the relative resistance of the potato cultivars under test. The relationship between the number of embryos in teneral adults and the production of nymphs by aphids was examined by grouping aphids in weight batches. There was a strong relationship between these two variables.     

Probiotic effects of beta-glucuronidase on the peach-potato aphid Myzus persicae (Aphididae)

beta-glucuronidase (GUS) is a reporter protein commonly expressed in transgenic plants allowing the visualization of the transformed individuals. In our recent work, we showed that consumption of transformed potato plants expressing this GUS enzyme improves performance of the phloem feeding aphid Myzus persicae. Those results led us to the conclusion that the expression of GUS in potato plants might be responsible for the probiotic effect measured in feeding aphids. In the present paper, artificial diets were used to provide active GUS (10 and 500 microg ml(-1)), inactivated heated GUS (500 microg ml(-1)), glucuronic acid (10, 100 and 500 microg ml(-1)), and bovine serum albumin (500 microg ml(-1)) to M. persicae. Our results reveal that these chemicals provided as food intake might influence the biological parameters of this aphid. Experiments showed a probiotic effect of 500 microg ml(-1) GUS diet, resulting in reduced larval mortality, and increased adult reproduction period and fecundity, which led to an increased population growth potential (r(m)=0.17+/-0.01 versus r(m)=0.12+/-0.03 for aphids fed on control diet). A lower amount of added GUS led to fewer variations, biological parameters being only slightly altered (r(m)=0.14+/-0.03). Statistically similar alterations of the biological parameters were obtained when comparing aphids fed on the diet added with inactivated GUS or the non-structural bovine serum albumin protein (r(m)=0.15+/-0.02 and 0.14+/-0.03, respectively). Feeding assays conducted with glucuronic acid supplemented diets enhanced longevity and nymph production of the adult aphids and reduced larval mortality, resulting in r(m)=0.15+/-0.02 for the highest dose (500 microg ml(-1)). Although 100 microg ml(-1) glucuronate diet did not induce any effect on M. persicae (r(m)=0.12+/-0.03), aphids fed on 10 microg ml(-1) glucuronate diet exhibited unexpected reduced demographic parameters (r(m)=0.10+/-0.03). Immuno-histological analysis showed GUS labeling along the whole digestive epithelium of adults and in various tissues including embryos and bacteriocytes. These results suggest that GUS crosses through the digestive tract. Western blots performed with protein extracts of transformed potato plants expressing the gus gene showed a unique band of molecular weight 76 kDa. On the contrary, in extracts from aphids fed on transgenic potato plants or bred on GUS 500 microg ml(-1) artificial diet, several proteins of lower molecular weight were hybridized, revealing proteolysis of ingested GUS. It is concluded that GUS protein, and more precisely GUS activity, is responsible for the probiotic effects on aphid feeding. The possible pathways of induction of such physiological alterations by GUS are discussed.     

Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae

The ecological consequences of genetic variability in host plant exploitation of Myzus persicae (Hemiptera, Aphididae) were studied in several agro-ecosystems, differing in crop plant heterogeneity. An analysis of aphid populations sampled from sugar beet, potatoes, and lettuce revealed changes in the frequency distribution of aphid clones according to their respective host plant adaptations. The spatial unit of differentiation was below an average field size of 3–5 hectares and a differentiation could be found in the centre of potato and sugar beet fields but not at the edge of the fields. On a temporal scale, the differentiation of populations is transitory even on a large-scale basis of highly specialized cropping areas. The ecological parameters of differentiation are discussed with special reference to agro-ecosystems and integrated pest management. Increasing the genetic heterogeneity of crop fields may help to reduce population outbreaks.

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Zusammenfassung Die ökologischen Konsequenzen genetischer Variabilität in der Wirtspflanzennutzung von Myzus persicae (Hemiptera, Aphididae) wurden in mehreren Agro-Ökosystemen untersucht, die sich in der Kulturpflanzenheterogenität unterscheiden. Eine Analyse von auf Rüben, Kartoffeln und Salat siedelnden Populationen zeigte eine genetische Differenzierung in Wirtspflanzen-angepaßte Feld-populationen. Die räumliche Einheit solcher Differenzierungen liegt unterhalb einer Feldgröße von 3–5 ha. Eine Differenzierung konnte hier in der Mitte der Felder aber nicht am Rand festgestellt werden. Aus zeitlicher Sicht ist die Differenzierung selbst in großräumigen, spezialisierten Anbaugebieten nur vorübergehend feststellbar. Die ökologischen Parameter der Differenzierung werden besonders in Hinsicht auf die integrierte Schädlingsbekämpfung in Agro-ökosystemen diskutiert. Eine Erhöhung der genetischen Heterogenität von Kulturpflanzenbeständen kann möglicherweise zu einer Verringerung von Blattlaus-Massenvermehrungen beitragen.

     

The inheritance of natural chromosomal polymorphisms in the aphid Myzus persicae (Sulzer)

Two types of chromosomal abnormality have been found in natural populations of Myzus persicae in Japan. One type is apparently due to an autosome 3 dissociation, giving a 2n=13 karyotype. The other is interpreted as a translocation between autosomes 1 and 3, resulting in a 2n=12 complement with marked structural heterozygosity. In laboratory crosses, both types of abnormality were inherited through the sexual phase. The proportions of each type in the F₁ agreed well with expectations, except that no forms homozygous for the translocation were obtained from crosses between translocation heterozygotes, and no karyotypes with both the translocation and the dissociation were obtained when translocated and dissociated forms were crossed. In the F₁ of one cross a triploid clone with the autosomal 1,3 translocation was obtained.     

Organic farming-compatible insecticides against the aphid Myzus persicae (Sulzer) in peach orchards

Abstract:  Three products allowed in organic farming (kaolin, mineral oil and insecticidal soap) as alternatives to chemical insecticides, were evaluated for the control of Myzus persicae (Sulzer) in a peach orchard. Their efficacy was compared with the neonicotinoid imidacloprid and an untreated control. The experiment was replicated for 2 years (2003 and 2004). The products were applied once in May every year and aphid infestation was recorded three to four times post-treatment. In 2004, the effect of the products on the predatory coccinellid species was also recorded. In 2003, all four products showed good control with average Abbott's efficiency ranging from 80% to 88%. In the next year, however, the products were less effective and only imidacloprid and kaolin reduced aphid population significantly compared with the untreated control, with an average Abbott's efficiency of 62% and 31%, respectively. This reduced efficiency was attributed to high rainfall occurring post-treatment. Regarding the effects on beneficial coccinellids, only imidacloprid and mineral oil reduced their numbers after application. The results showed that the three alternative products and especially kaolin are promising for aphid control in peach orchards. Kaolin has also low side-effects on beneficials and it could be used in organic peach orchards.     

Microsatellite variation in cyclically parthenogenetic populations of Myzus persicae in south-eastern Australia

We examined the population structure of the introduced aphid, Myzus persicae collected mainly from its primary host, Prunus persica, in south-east Australia. Myzus persicae has been present in Australia since at least 1893. Samples were collected in the spring of 1998 from two mainland and three Tasmanian localities and isofemale lines were established in the laboratory. The reproductive mode (life cycle), karyotype and 17-locus microsatellite genotype of each clone were determined. All populations showed significant population differentiation (F(ST) 0.058-0.202) even over small geographic distances (<50 km). All clones were karyotypically normal except for a subset of clones from one site that was exposed to the carbamate insecticide, Pirimor, the week prior to sampling. Those clones were heterozygous for an autosomal 1,3 translocation frequently associated in M. persicae with insecticide resistance. In contrast to other loci and despite being on different chromosomes, loci myz2(A) and M55(A) showed general and significant linkage disequilibrium. These loci may be affected by epistatic selection. We discuss the observed high clonal diversity, moderate but significant population differentiation, general conformance to Hardy-Weinberg equilibria and low linkage disequilibria with particular focus on the global population biology of M. persicae.     

Temporal dynamics of genotypic diversity reveal strong clonal selection in the aphid Myzus persicae

Parthenogenetic organisms often harbour substantial genotypic diversity. This diversity may be the result of recurrent formations of new clones, or it may be maintained by environmental heterogeneity acting on ecological differences among clones. In aphids, both processes may be important because obligate and cyclical parthenogens can form mixed populations. Using microsatellites, I analysed the temporal dynamics of clonal diversity in such a population of the aphid Myzus persicae over a 1-year period. The frequency distribution of clonal genotypes was very skewed, with many rare and few common clones. The relative frequencies of common clones underwent strong and rapid changes indicative of intense clonal selection. Differences in their host associations suggest that these shifts may partly be caused by changes in the abundance of annual host plants. Other selective factors of potential importance are also discussed. New, sexually produced genotypes made a minor contribution to clonal diversity, consistent with the observed heterozygote excess characteristic of predominantly asexual populations in M. persicae.     

Factors affecting the activity of alatae of the aphids Myzus persicae (Sulzer) and Brevicoryne brassicae (L.)

Apparatus was designed for testing the frequency of flights of aphids under different conditions of temperature, relative humidity, light and pressure. Young aphids (1–4 days after metamorphosis) flew more often and showed less individual variability than older ones; with all ages activity increased for the first few hours under experimental conditions. Starving increased activity for the first 1–2 hr. Aphids used in experiments on a second day flew less frequently than controls which had remained on the plant the first day. Alate B. brassicae were more active than M. persicae : both species showed alternating periods of activity and quiescence.
At light intensities between 100 and 1000 f.c. there was little difference in flight frequency, but below 100 f.c. activity declined rapidly and apparently ceased with darkness.
Changes in relative humidity temporarily affected flight frequency, a change to a higher humidity retarding, a change to a lower increasing it. After adjusting to the change aphids flew readily at all humidities tested between 50 and 100% with temperatures below 80° F. (26.7°C.). The combination of high humidity and high temperature (90°F. = 32·2°C.) sometimes inhibited flight.
Changes of pressure often increased activity temporarily and flight frequency was greater under fluctuating pressure than under constant pressure.
It is concluded that changes in microclimate in crops are adequate to influence frequency of flight of aphids and consequently the spread of virus diseases.     

Duplication of the Rdl GABA receptor subunit gene in an insecticide-resistant aphid, Myzus persicae

Resistance to cyclodiene insecticides is associated with replacements of a single amino acid (alanine 302) in a γ-aminobutyric acid (GABA) receptor subunit encoded by the single-copy gene Resistance to dieldrin (Rdl). Alanine 302 is predicted to reside within the second membrane-spanning region of the Rdl receptor, a region that is thought to line the integral chloride ion channel pore. In all cyclodiene-resistant insects studied to date, this same alanine residue is replaced either by a serine, or, in some resistant strains of Drosophila simulans, a glycine residue. Therefore, individuals can carry only two different Rdl alleles. In contrast, here we report the presence of up to four different Rdl-like alleles in individual clones of the green peach aphid, Myzus persicae. In addition to the wild-type copy of Rdl gene (encoding A302 or allele A), M. persicae carries three other alleles with the following amino acid replacements: A302?→?Glycine (allele G), A302?→ Serine^TCG (allele S) and A302?→?Serine^AGT (allele S′). Evidence from direct nucleotide sequencing and Single Stranded Conformational Polymorphism (SSCP) analysis shows that at least three of these different Rdl alleles (i.e. A, G and S) are commonly present in individual aphids or aphid clones. Southern analysis using allele-specific probes and analysis of sequences downstream of the exon containing the resistance-associated mutation confirm the presence of two independent Rdl-like loci in M. persicae. One locus carries the susceptible alanine (A) and/or resistant glycine (G) allele while the other carries the two serine alleles (S or S′). Whereas resistance levels are correlated with the glycine replacement, the S allele was present in all aphid clones, regardless of their resistance status. These results suggest that target site insensitivity is associated with replacements at the first (A/G) but not the second (S/S′) locus. Phylogenetic analysis of nucleotide sequences indicates that both putative aphid Rdl loci are monophyletic with respect to other insect Rdl genes and may have arisen through a recent gene duplication event. The implications of this duplication with respect to insecticide resistance and insect GABA receptor subunit diversity are discussed.     

Long-term effects of elevated CO2 and temperature on populations of the peach potato aphid Myzus persicae and its parasitoid Aphidius matricariae

Model terrestrial ecosystems were set-up in the Ecotron controlled environment facility. The effects of elevated CO₂ (ambient + 200 mol/mol) and temperature (ambient + 2.0°C) on plant chemistry, the abundance of the peach potato aphid Myzus persicae, and on the performance of one of its parasitoids Aphidius matricariae, were studied. Total above-ground plant biomass at the end of the experiment was not affected by elevated atmospheric CO₂, nor were foliar nitrogen and carbon concentrations. Elevated temperature decreased final plant biomass while leaf nitrogen concentrations increased. Aphid abundance was enhanced by both the␣CO₂ and temperature treatment. Parasitism rates remained unchanged in elevated CO₂, but showed an increasing trend in conditions of elevated temperature. Our results suggest that M. persicae, an important pest of many crops, might increase its abundance under conditions of climate change. Received: 26 January 1998 / Accepted: 20 April 1998     

Effects of acclimation and latitude on the activity thresholds of the aphid Myzus persicae in Europe

Activity thresholds were measured in nine anholocyclic clones of the peach‐potato aphid Myzus persicae collected along a latitudinal cline of its European distribution from Sweden to Spain. The effects of collection origin and intra‐ and intergenerational acclimation on these thresholds were investigated. Low‐temperature (10°C) acclimation for one generation depressed the movement threshold and chill coma temperatures, with the largest reduction in movement threshold recorded for clone UK 1 (8.8–2.5°C) and in chill coma for UK 2 (4.8–2.0°C). High‐temperature (25°C) acclimation for one generation increased the heat movement threshold and heat coma temperature with the largest increase in the movement threshold (40.1–41.1°C) and heat coma (41.4–42.3°C) recorded for clone Swed 1. There was no further intergenerational acclimation over three generations. High‐temperature activity thresholds were less plastic than low‐temperature thresholds, and, consequently, thermal activity ranges were expanded following low‐temperature acclimation. No constant affect of acclimation was observed on chill coma recovery, although clonal differences were observed with Swed 1 and 3 requiring some of the longest complete recovery times. There was no relationship between latitude and activity thresholds with the exception of heat coma data where Scandinavian clones Swed 2 and 3 consistently displayed some of the lowest heat coma temperatures (e.g. 41.3°C for both clones at 20°C) and Mediterranean clones Span 1, 2 and 3 displayed some of the highest (e.g. 42.1, 41.9 and 42.5°C, respectively, at 20°C). These data suggest that clonal mixing could occur over a large scale across Europe, limiting local adaptation to areas where conditions enable long‐term persistence of populations, e.g. adaptation to higher temperatures in the Mediterranean region. It is suggested that aphid thermal tolerance could be governed more by clonal type than the latitudinal origin.     

Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape

In fall, Myzus persicae (Sulzer) (Homoptera: Aphididae) may exhibit population resurgence in winter oilseed rape in France. This resurgence may arise from pyrethroid treatments against Coleoptera (Psylliodes chrysocephala L.) that either kill parasitoids present during treatment or prevent recolonization by off-crop parasitoids. We studied the impact of Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae) on populations of M. persicae when parasitoids were introduced on deltamethrin-treated plants at increasing intervals after treatment. Parasitoids were introduced 1, 2, 7, or 14 d posttreatment on individually caged plants infested with established populations of M. persicae. Aphids were counted 7, 14 and 21 d after parasitoid introduction. First, we observed that both the pesticide and the parasitoid reduced aphid population growth and that their effects were additive. Second, there was no mortality of parasitoids exposed to treated leaves in a device with a refuge area, and only 20% of mortality without the refuge area. Furthermore, deltamethrin residues had no effect on the reproduction of D. rapae females. Compared with the known toxicity of deltamethrin to D. rapae on glass, this low mortality may have been due to both the high liposolubility of deltamethrin (leading to a rapid diffusion of residues in the oilseed rape leaf cuticle) and to the existence of a refuge area. This work suggests that D. rapae could limit populations of M. persicae in the fall, even after pyrethroid treatment, because the presence of deltamethrin residues had little impact on the parasitoid.     

Within-species variability of the response to 20-hydroxyecdysone in peach-potato aphid (Myzus persicae Sulzer)

Phytoecdysteroids have been proposed as new tools for controlling crop pests because of their endocrine disruption and deterrent effects on insects and nematodes. There is increasing evidence of variability between taxa in sensitivity to phytoecdysteroids, but the genetic variability of this sensitivity within species is unknown. However, knowledge about this intraspecies variability is required for predicting evolution of the pest's response to new control methods. We assessed the variability of the response of the aphid Myzus persicae Sulzer, a major agricultural pest, to 20-hydroxyecdysone (20E). We determined the number of nymphs produced by six clones of M. persicae exposed to various concentrations of 20E and the capacity of these clones to detect 20E in choice experiments. High concentrations of 20E significantly decreased the number of nymphs produced for two clones and both increases and decreases in the number of offspring were detected at low concentrations. Two clones significantly avoided food with 20E, while one significantly preferred it, suggesting that 20E does not always act as a deterrent in this species. We conclude that genetic variability in the response to 20E exists in natural populations of M. persicae. The consequences of this finding on the sustainability of control methods using 20E are discussed.     

Failure of the aphid, Myzus persicae, to compensate for poor diet during early growth

ABSTRACT. Compensation in mean relative growth rate of M. persicae occurred when aphids normally kept on susceptible brussels sprout plants were starved for only 2 h daily or kept on 'resistant' plants (given low nitrogen:high potassium fertilization) for 48 h. More adverse conditions, e.g. 4 or 8 h daily starvation, 48 h on leaf discs or 60 h on 20% sucrose, resulted in a low aphid growth rate being maintained on transfer to susceptible plants. The low overall growth rate could not be explained in terms of a weight loss by the aphid at any stage and is assumed to be a behavioural phenomenon. It is concluded that it is unwise, in the study of aphid—plant relationships, to rely on pre-conditioning aphids in poor conditions with the hope that this might magnify differences in subsequent aphid response.     

Comparative analysis of Solanum stoloniferum responses to probing by the green peach aphid Myzus persicae and the potato aphid Macrosiphum euphorbiae

Abstract Plants protect themselves against aphid attacks by species‐specific defense mechanisms. Previously, we have shown that Solanum stoloniferum Schlechtd has resistance factors to Myzus persicae Sulzer (Homoptera: Aphididae) at the epidermal/mesophyll level that are not effective against Macrosiphum euphorbiae Thomas (Homoptera: Aphididae). Here, we compare the nymphal mortality, the pre‐reproductive development time, and the probing behavior of M. persicae and M. euphorbiae on S. stoloniferum and Solanum tuberosum L. Furthermore, we analyze the changes in gene expression in S. stoloniferum 96 hours post infestation by either aphid species. Although the M. euphorbiae probing behavior shows that aphids encounter more probing constrains on phloem activities–longer probing and salivation time– on S. stoloniferum than on S. tuberosum, the aphids succeeded in reaching a sustained ingestion of phloem sap on both plants. Probing by M. persicae on S. stoloniferum plants resulted in limited feeding only. Survival of M. euphorbiae and M. persicae was affected on young leaves, but not on senescent leaves of S. stoloniferum. Infestation by M. euphorbiae changed the expression of more genes than M. persicae did. At the systemic level both aphids elicited a weak response. Infestation of S. stoloniferum plants with a large number of M. persicae induced morphological changes in the leaves, leading to the development of pustules that were caused by disrupted vascular parenchyma and surrounding tissue. In contrast, an infestation by M. euphorbiae had no morphological effects. Both plant species can be regarded as good host for M. euphorbiae, whereas only S. tuberosum is a good host for M. persicae and S. stoloniferum is not. Infestation of S. stoloniferum by M. persicae or M. euphorbiae changed the expression of a set of plant genes specific for each of the aphids as well as a set of common genes.