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Host-associated populations in the lettuce root aphid, Pemphigus bursarius (L.).

Pemphigus bursarius is a host-alternating aphid in which annual rounds of sexual reproduction on its primary host, Populus nigra, are interspersed with parthenogenesis on a range of secondary hosts. Evidence was sought for the existence of genetically distinct populations, associated with different secondary hosts, in P. bursarius. Microsatellite markers revealed that genetically distinct populations were present on three different secondary host species. Microsatellites were also used, in conjunction with mitochondrial DNA sequence variation, to investigate the relationships between aphids on Populus, following sexual reproduction, and those on the secondary hosts. Evidence was found for a distinct, cyclically parthenogenetic population that exploited Lactuca sativa as its secondary host. In contrast, populations associated with Matricaria inodora appeared to be largely composed of obligate parthenogens or may even have been another species of Pemphigus. Populations on Lapsana communis appeared to be a mixture of cyclical and obligate parthenogens and were more genetically heterogeneous than those on other secondary hosts, possibly due to founder effects. Experiments to measure the performance of P. bursarius clones on different secondary hosts were inconclusive, failing to demonstrate either the presence or absence of adaptations to secondary hosts.

Animals↗

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.

Agriculture↗

Does insecticide resistance alone account for the low genetic variability of asexually reproducing populations of the peach-potato aphid Myzus persicae?

The typical life cycle of aphids includes several parthenogenetic generations and a single sexual generation (cyclical parthenogenesis), but some species or populations are totally asexual (obligate parthenogenesis). Genetic variability is generally low in these asexually reproducing populations, that is, few genotypes are spread over large geographic areas. Both genetic drift and natural selection are often invoked to account for this low genetic variability. The peach-potato aphid, Myzus persicae, which encompasses both cyclical and obligate parthenogens, has developed several insecticide resistance mechanisms as a consequence of intense insecticide use since the 1950s. We collected asexually reproducing M. persicae from oilseed rape and examined genetic variability at eight microsatellite loci and three insecticide resistance genes to determine whether their genetic structure was driven by drift and/or selection. We identified only 16 multilocus microsatellite genotypes among 255 individuals. One clone, which combined two insecticide resistance mechanisms, was frequently detected in all populations whatever their location over a large geographical area (the northern half of France). These unexpected findings suggest that drift is not the unique cause of this low variability. Instead, the intensification of both insecticide treatments and oilseed rape cultivation may have favored a few genotypes. Thus, we propose that selective pressures resulting from human activities have considerably modified the genetic structure of M. persicae populations in northern France in a relatively short period of time.

Alleles↗

Chromosomal stasis versus plasmid plasticity in aphid endosymbiont Buchnera aphidicola.

The study of three genomes of the aphid endosymbiont Buchnera aphidicola has revealed an extraordinary stasis: conservation of gene order and genetic composition of the chromosome, while the chromosome size and number of genes has reduced. The reduction in genome size appears to be ongoing since some lineages we now know to have even smaller chromosomes than the first B. aphidicola analysed. The current sequencing by our group of one of these smaller genomes with an estimated size of 450 kb, and its comparison with the other three available genomes provide insights into the nature of processes involved in shrinkage. We discuss whether B. aphidicola might be driven to extinction and be replaced by secondary aphid endosymbionts. In some lineages, genes encoding key enzymes in the pathways leading to tryptophan and leucine biosynthesis (trpEG and leuABCD, respectively) are located on plasmids, rather than the main chromosome. In contrast to the stasis of the main chromosome, plasmid genes have frequently been transferred to the main chromosome and undergone other gene rearrangements. We propose a two-step scenario to explain these contrasting modes of evolution. Essential genes may have escaped regulation by moving to plasmids in a moving B. aphidicola ancestor. B. aphidicola became polyploidy at a given stage of its evolution and plasmid genes have been transferred to the main chromosome through several independent events.

Animals↗

Wing dimorphism in aphids.

Many species of insects display dispersing and nondispersing morphs. Among these, aphids are one of the best examples of taxa that have evolved specialized morphs for dispersal versus reproduction. The dispersing morphs typically possess a full set of wings as well as a sensory and reproductive physiology that is adapted to flight and reproducing in a new location. In contrast, the nondispersing morphs are wingless and show adaptations to maximize fecundity. In this review, we provide an overview of the major features of the aphid wing dimorphism. We first provide a description of the dimorphism and an overview of its phylogenetic distribution. We then review what is known about the mechanisms underlying the dimorphism and end by discussing its evolutionary aspects.

Animals↗

Cloning and analysis of the esterase genes conferring insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer).

Full-length cDNA clones encoding the esterases (E4 and FE4) that confer insecticide resistance in the peach-potato aphid [Myzus persicae (Sulzer)] were isolated and characterized. The E4 cDNA contained an open reading frame of 1656 nucleotides, coding for a protein of 552 amino acids. The FE4 cDNA shared 99% identity with E4 over this region, the most important difference being a single nucleotide substitution resulting in the FE4 mRNA having an extra 36 nucleotides at the 3' end. The derived amino acid sequences for the N-terminus of E4 and FE4 were identical, with the first 23 residues being characteristic of a signal peptide and the next 40 residues being an exact match to the N-terminal sequence determined by Edman degradation of both purified proteins. The predicted molecular masses of 58.8 and 60.2 kDa for the E4 and FE4 polypeptides were consistent with those previously observed by in vitro translation of mRNA. Five potential N-linked glycosylation sites were present in both polypeptides, in accordance with earlier evidence that the native esterases are glycoproteins. Comparison of the aphid esterase protein sequences with other serine hydrolases provided evidence that their activity involves a charge-relay system with a catalytic triad the same as that found in acetylcholinesterase. Restriction mapping and sequencing of cloned genomic DNA showed that the E4 gene is spread over 4.3 kb with six introns and that the previously reported differences between the 3' ends of the E4 and FE4 genes result from single nucleotide substitutions and not gross differences in the DNA sequences.

Amino Acid Sequence↗

Structure and organization of amplicons containing the E4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer).

Insecticide resistance in the aphid Myzus persicae results primarily from the amplification of genes encoding the insecticide-detoxifying esterase, E4. Here we report the analysis of flanking DNA co-amplified with the E4 gene. The 5' end of this gene has an untranslated leader sequence interspersed by two introns, and the promoter region lacks TATA and CAAT boxes. The DNA breakpoint involved in the generation of the amplification is just upstream (approx. 250 bp) of the putative E4 transcription start site; thus the E4 gene is very close to the 5' end of the approx. 24 kb amplicon. PCR primers specific to the 'novel joint' generated during the amplification have been used to show that a wide range of aphid clones have the same amplicons, arranged as a series of head-to-tail direct repeats. Long-distance mapping has revealed the structure of these repeats. This has important implications for understanding both the generation of the amplified genes and the origin and spread of insecticide resistance in M. persicae.

Animals↗

Evidence that the E4 and FE4 esterase genes responsible for insecticide resistance in the aphid Myzus persicae (Sulzer) are part of a gene family.

The amplification of genes encoding the esterases E4 and FE4 is a widespread mechanism of insecticide resistance in the peach-potato aphid, Myzus persicae (Sulzer). We present evidence that in susceptible aphids the two genes are adjacent to each other in a head-to-tail arrangement with E4 upstream of FE4 and with approx. 19 kb of intervening sequence. There are also at least two other closely related sequences which might come from other members of an esterase gene family, in line with reports of other insect gene families encoding detoxifying enzymes. The close identity between E4 and FE4 genes indicates a recent duplication and divergence. The subsequent amplifications giving multiple copies of either E4 or FE4 must have involved two separate events, each probably occurring once and then being selected by insecticide exposure and spread by migration. The cloning of sequences upstream of the FE4 gene suggest, by comparison with E4, that the two genes are regulated in different ways. FE4 has sequences corresponding to a conventional promoter (TATA box and CAP site) that are not present in E4; on the other hand, FE4 lacks the CpG island present 5' of E4 genes that may control expression through changes in DNA methylation. The differences are likely to have occurred by the duplication event that gave rise to E4 and FE4 leading to different 5' sequences.

Animals↗

Methylation and expression of amplified esterase genes in the aphid Myzus persicae (Sulzer).

Most populations of the aphid Myzus persicae have amplified genes (up to 80 copies) encoding the insecticide-detoxifying esterase E4. This paper reports the analysis of methylation of the E4 gene and its flanking DNA with the use of methylation-sensitive restriction enzymes, CpG profiling and bisulphite sequencing. In combination these show that E4 has 5-methylcytosine confined to CpG doublets, as previously shown for vertebrate genomes; this is the first such report for an insect gene. The methylation is present within the gene but absent from upstream regions, including the 5' CpG-rich region around the start of transcription, and from 3' flanking DNA. Methylated E4 genes are expressed; loss of the 5-methylcytosine is correlated with a loss of transcription, although this is not accompanied by a global loss of the 5-methylcytosine present in the aphid genome. These results suggest that the methylation of E4 has a positive role in expression, and call into question the widely held view that methylation in invertebrate genomes is confined to regions that do not contain genes and that methylation is always associated with gene silencing.

Animals↗

Low genetic diversity among pea aphid (Acyrthosiphon pisum) biotypes of different plant affiliation.

Genetic diversity in the pea aphid Acyrthosiphon pisum was investigated by a restriction fragment length polymorphism (RFLP) analysis of three maternally inherited genomes (mitochondrial DNA and plasmids of the symbiotic bacteria Buchnera). Twenty-nine parthenogenetic clones of three A. pisum biotypes, defined by their capacity to use the legume crops pea, alfalfa and red clover, respectively, were analysed, and a total of 67 restriction sites was scored. No restriction site variation in the mitochondrial genome was obtained, but length variation at two regions (the A + T-rich region and ND3-ND5 region) was noted. One aphid clone bore a variant HindIII restriction site in the Buchnera leucine plasmid (pAPEleu), and two clones were heteroplasmic for a 0.76-kb deletion in the Buchnera tryptophan plasmid (pAPEtrp). Based on arthropod nucleotide substitution rates, it is proposed that the crop-feeding biotypes of A. pisum may have diversified within the last 100 000 years and possibly much more recently, since the advent of agriculture.

Animals↗

Environmentally related patterns of reproductive modes in the aphid Myzus persicae and the predominance of two 'superclones' in Victoria, Australia.

Asexual organisms that naturally coexist with sexual relatives may hold the key to understanding the maintenance of sex and recombination, a long-standing problem in evolutionary biology. This situation applies to the peach-potato aphid, Myzus persicae, in southeastern Australia where cyclical parthenogens form mixed populations with obligate parthenogens. We collected M. persicae from several areas across Victoria, genotyped them at seven microsatellite loci and experimentally determined their reproductive mode. The geographic distribution of reproductive modes was correlated with two environmental variables that differentially affect obligate and cyclical parthenogens; obligate parthenogens were less frequent in areas with cold winters because they cannot produce frost-resistant eggs while cyclical parthenogens were limited by the availability of their primary host, peach, on which sexual reproduction takes place. Clonal diversity increased with the proportion of cyclical parthenogens in a sample because they tended to have unique microsatellite genotypes, whereas many obligate parthenogens were copies of the same genotype. Two obligately asexual genotypes stood out as being very abundant and widespread, one constituting 24% and the other 17.4% of the entire collection. Both of these highly successful genotypes were present in the majority of all collection sites. Genetic population structure was weak, albeit significant, with a multilocus FST of only 0.021 when samples were reduced to only one representative of each genotype. Interestingly, obligate parthenogens were, on average, more heterozygous and exhibited larger allele size differences between the two alleles at individual loci than cyclical parthenogens. This striking pattern could result from hybridization, for which we have no evidence, or may reflect the previously proposed model of biased mutational divergence of microsatellite alleles within asexual aphid lineages.

Animals↗

Experimental epizootiology of Zoophthora anhuiensis (Entomophthorales) against Myzus persicae (Homoptera: Aphididae) with a description of a modified Gompertz model for aphid epizootics.

Epizootiological features of Zoophthora anhuiensis, a fungal pathogen specific to aphids in southern China, were studied in six aptera colonies of Myzus persicae at 16 regimes of temperature (T = 10, 15, 20 and 25 degrees C) and relative humidity (H = 90%, 95%, 98% and 100% RH) with initially infected proportion (Ip) of 0.5 in experiment (Expt) 1 or at a fixed regime of 15 degrees C and 100% RH with a variable Ip of 0.17-1.00 in Expt 2. Mycosis-caused mortalities (Mp) varied with aphid densities (D) over time after colony initiation (t) were well fitted to a Gompertz growth model modified to include the variables T, H, Ip and D in the form of Mp = 91.72exp[-5.282exp[-(0.0095T + 0.0128H/T-0.5407D2/H)t]] for Expt 1 (r2 = 0.94) or Mp = 95.49exp[-4.314exp[-(0.1479Ip + 0.1636/D)t]] for Expt 2 (r2 = 0.97). These variables were effective in determining the rate of epizootic development in the M. persicae colonies. Based on the observed and fitted results, Z. anhuiensis was most adaptive to cool climate or season and epizootiologically was subject to a minimal effect of RH at an optimum of approximately 15 degrees C. However, the humidity became determinant for epizootic progress at higher temperatures. Interactive effects of the variables and application of the fitted models for predicting epizootic development in field situations are discussed.

Animals↗

Hydroperoxide lyase depletion in transgenic potato plants leads to an increase in aphid performance.

Hydroperoxide lyases (HPLs) catalyze the cleavage of fatty acid hydroperoxides to aldehydes and oxoacids. These volatile aldehydes play a major role in forming the aroma of many plant fruits and flowers. In addition, they have antimicrobial activity in vitro and thus are thought to be involved in the plant defense response against pest and pathogen attack. An HPL activity present in potato leaves has been characterized and shown to cleave specifically 13-hydroperoxides of both linoleic and linolenic acids to yield hexanal and 3-hexenal, respectively, and 12-oxo-dodecenoic acid. A cDNA encoding this HPL has been isolated and used to monitor gene expression in healthy and mechanically damaged potato plants. HPL gene expression is subject to developmental control, being high in young leaves and attenuated in older ones, and it is induced weakly by wounding. HPL enzymatic activity, nevertheless, remains constant in leaves of different ages and also after wounding, suggesting that posttranscriptional mechanisms may regulate its activity levels. Antisense-mediated HPL depletion in transgenic potato plants has identified this enzyme as a major route of 13-fatty acid hydroperoxide degradation in the leaves. Although these transgenic plants have highly reduced levels of both hexanal and 3-hexenal, they show no phenotypic differences compared with wild-type ones, particularly in regard to the expression of wound-induced genes. However, aphids feeding on the HPL-depleted plants display approximately a two-fold increase in fecundity above those feeding on nontransformed plants, consistent with the hypothesis that HPL-derived products have a negative impact on aphid performance. Thus, HPL-catalyzed production of C6 aldehydes may be a key step of a built-in resistance mechanism of plants against some sucking insect pests.

Aldehyde-Lyases↗

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.

Acetylcholinesterase↗

Diet breadth and its relationship with genetic diversity and differentiation: the case of southern beech aphids (Hemiptera: Aphididae).

Herbivorous insect species with narrow diet breadth are expected to be more prone to genetic differentiation than insect species with a wider diet breadth. However, a generalist can behave as a local specialist if a single host-plant species is locally available, while a specialist can eventually behave as a generalist if its preferred host is not available. These problems can be addressed by comparing closely related species differing in diet breadth with overlapping distributions of insect and host populations. In this work, diet breadth, genetic diversity and population differentiation of congeneric aphid species from southern beech forests in Chile were compared. While at the species level no major differences in genetic diversity were found, a general trend towards higher genetic diversity as diet breadth increased was apparent. The aphid species with wider diet breadth, Neuquenaphis edwardsi (Laing), showed the highest genetic diversity, while the specialist Neuquenaphis staryi Quednau & Remaudière showed the lowest. These differences were less distinct when the comparisons were made in the same locality and over the same host. Comparison of allopatric populations indicates that genetic differentiation was higher for the specialists, Neuquenaphis similis Hille Ris Lambers and N. staryi, than for the generalist N. edwardsi. Over the same host at different locations, genetic differentiation among populations of N. edwardsi was higher than among populations of N. similis. The results support the assumption that specialists should show more pronounced genetic structuring than generalists, although the geographical distribution of host plants may be playing an important role.

Animals↗

Dynamics of production of sexual forms in aphids: theoretical and experimental evidence for adaptive "coin-flipping" plasticity.

The best strategy for an organism to deal with unpredictable environmental conditions is a stochastic one, but it is not easy to distinguish it from nonadaptive randomness in phenotype production, and its convincing demonstrations are lacking. Here we describe a new method for detection of adaptive stochastic polyphenism and apply it to the following problem. In fall, each female of the bird cherry-oat aphid, Rhopalosiphum padi, faces a decision either to produce sexuals, which mate and lay cold-tolerant eggs, or to continue production of cold-sensitive parthenogenetic females, which potentially yields a higher population growth rate but is risky because a cold winter can kill all of her descendants. Using a simulation model, we show that global investment in sexual reproduction should be proportional to winter severity and that variance in the peak date of production of sexual individuals should depend on climate predictability. Both predictions are validated against standardized trap data on aphid flight accompanied by meteorological data, and the predictions support adaptive phenotypic plasticity.

Adaptation, Physiological↗

Microsatellite and chromosome evolution of parthenogenetic sitobion aphids in Australia.

Single-locus microsatellite variation correlated perfectly with chromosome number in Sitobion miscanthi aphids. The microsatellites were highly heterozygous, with up to 10 alleles per locus in this species. Despite this considerable allelic variation, only seven different S. miscanthi genotypes were discovered in 555 individuals collected from a wide range of locations, hosts and sampling periods. Relatedness between genotypes suggests only two successful colonizations of Australia. There was no evidence for genetic recombination in 555 S. miscanthi so the occurrence of recent sexual reproduction must be near zero. Thus diversification is by mutation and chromosomal rearrangement alone. Since the aphids showed no sexual recombination, microsatellites can mutate without meiosis. Five of seven microsatellite differences were a single repeat unit, and one larger jump is likely. The minimum numbers of changes between karyotypes corresponded roughly one-to-one with microsatellite allele changes, which suggests very rapid chromosomal evolution. A chromosomal fission occurred in a cultured line, and a previously unknown chromosomal race was detected. All 121 diverse S. near fragariae were heterozygous but revealed only one genotype. This species too must have a low rate of sexual reproduction and few colonizations of Australia.

Animals↗

Categories of resistance at four growth stages in three wheats resistant to the Russian wheat aphid (Homoptera: Aphididae).

Laboratory experiments were conducted to determine categories of resistance to Russian wheat aphid, Diuraphis noxia (Mordvilko), in three wheats, Triticum aestivum L, (PI 372129, PI 243781, and PI 222668) at Zadoks growth stages 10, 20, 30, and 40. 'TAM 107' was used as the susceptible standard. Antixenosis was observed in PI 222668 and PI 372129. Antibiosis was expressed as reduced nymphipositional period, daily nymph production, and fecundity at the jointing (Zadoks 30) and boot (Zadoks 40) stages in PI 243781 and at tillering (Zadoks 20) in TAM 107. Antibiosis, expressed as reduced intrinsic rate of increase, was observed in PI 222668 at tillering (Zadoks 20). Tolerance to chlorosis and leaf rolling was expressed in the three resistant wheats at all growth stages tested. Tiller production, floret formation, spike length and wet weight were affected by Russian wheat aphid feeding after Zadoks 10. Reduction in spike length did not occur in PI 372129 and PI 243781.

Animals↗