Genotypic variation in propensity for host alternation within a population of Pemphigus betae (Homoptera: Aphididae)

In a Utah canyon, the aphid Pemphigus betae shows both a complex life cycle, with alternation between a gall-forming phase on cottonwood leaves and a root-feeding phase on herbs, and a simple life cycle, with year-round residence on roots. In order to determine the extent of clonal variation in life cycle, experiments using multiple sublines of individual clones were carried out in the laboratory and in the field. Previous studies suggested that both genetic and environmental factors underlie life cycle differences among subpopulations of aphids from different sites and different life cycle phases. The current study is the first assessment of clonal variation in propensity for host alternation within a natural population of aphids. In the laboratory experiment, clones showed highly significant differences in reproductive rates and in production of the host-alternating migrants. In agreement with previous findings, clones originating from lineages that had alternated to cotton-wood hosts in the previous year had lower average density and produced more migrants than clones originating from lineages that had remained on roots during the previous year. In order to ascertain how clonal variation and site-specific environmental factors affect life cycle variation under natural conditions, clones from laboratory cultures were used to establish experimental colonies at two elevational sites within the canyon. Production of the host-alternating migrants was affected strongly by clone-x-site interaction and was affected slightly by site. Results from both experiments indicate that loss of host alternation in P. betae could be effected through genetic change, environmental change, or both.     

PHENOTYPE FIXATION AND GENOTYPIC DIVERSITY IN THE COMPLEX LIFE CYCLE OF THE APHID PEMPHIGUS BETAE

The aphid Pemphigus betae typically shows a complex life cycle, with annual alternation between cottonwood trees, where it forms leaf galls, and herbaceous plants, where it lives on roots. Distinct phenotypes are associated with each phase. In a population in Utah, aphid clones vary in their tendencies to undergo the cottonwood phase of the life cycle, with certain clones rarely producing the winged migrants that initiate the cottonwood phase. To examine the extent of genotypic variability in life cycle traits and to determine the consequences of phase deletion for fitness in the remaining phase of the life cycle, I compared performances of sets of clones that differed in their tendencies to delete the cottonwood phase. Performances of 35 aphid clones were compared on root hosts in the laboratory, by quantifying size (a correlate of fecundity), developmental time, and mortality for clonal sublines. Clones that tend to delete the cottonwood phase and remain on roots developed faster, showed lower mortality, and were larger as compared to clones that tend to undergo an annual migration to cottonwood. These laboratory comparisons of individual clones agree with earlier findings from field experiments. Performance also varied significantly among clones within sets, with the set of clones not previously subjected to selection on root hosts showing higher variance than clones isolated following selection in the root-inhabiting phase. These data suggest that selection in the cottonwood phase opposes selection in the root phase. Thus, even in cases of polyphenism, in which divergent developmental pathways confer some independence of phenotypic expression in alternative phases, antagonistic pleiotropy limits adaptation within a phase. These findings on the correlates of intrapopulational variation in frequency of phase expression provide some of the best evidence for character release following reduction of a complex life cycle, and they support the hypothesis that the advantages of polyphenism may be limited by negative genetic correlations among fitness traits of alternative phenotypes.     

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.     

Body colour and genetic variation in winged morph production in the pea aphid

Aphids (Homoptera: Aphidoidea) produce a number of different phenotypes in their life-cycle, among which are winged (alate) and wingless (apterous) morphs. Lowe & Taylor (1964) and Sutherland (1969a, b) were the first to suggest that aphid clones differ in their propensity to produce the winged morph and that in the pea aphid (Acyrthosiphon pisum Harris), this propensity is linked to the colour of the phenotype. We tested for the occurrence of genetic variation in winged morph production by rearing individuals from red and green clones of pea aphid under wing-inducing (crowding) and control conditions, and scored the phenotypes of their offspring. Clones differed significantly in alate production and red clones produced on average a higher proportion of winged morphs than green clones. Importantly, however, there was considerable variation between clones of the same colour. Broad-sense heritabilities of winged morph production were 0.69 (crowding treatment) and 0.63 (control). Clones also differed in the number of offspring they produced. When exposed to the crowding stimulus, aphids deferred offspring production, resulting in a higher number of offspring produced in the crowding treatment than in the control.     

Performance of clones and morphs of two cereal aphids on wheat plants with high and low nitrogen content

The great variability of the aphid life cycle and their tendency for host alternation gives rise to aphid clones and morphs. Inter‐ and intraclonal variability may be observed in the responses of aphids to various environmental factors. In this study we aimed to evaluate the influence of intrinsic factors (clone and morph type) on the intrinsic rate of increase (r_m) of the English grain aphid, Sitobion avenae (Fabricius), and the bird cherry‐oat aphid, Rhopalosiphum padi (Linnaeus). For each species four apterous clones were collected from established laboratory colonies and compared to assess their relative fitness on high‐ and low‐nitrogen wheat plants under laboratory conditions. The clones had significantly different intrinsic rates of increase on high‐ and low‐nitrogen plants. All R. padi clones had a higher intrinsic rate of increase and mean relative growth rate than S. avenae. Experiments were also conducted to compare the mean fecundity of apterous and alate morphs of S. avenae and R. padi clones on high‐ and low‐nitrogen wheat plants. On high‐nitrogen plants the apterous morphs of S. avenae clones had significantly higher mean fecundity than alate morphs. There were no significant differences between the mean fecundity of alate morphs of the same species on high‐ and low‐nitrogen plants. The results support the idea of better fitness of specific clones/morphs on certain host plants due to higher and lower intrinsic rates of increase.     

EVOLUTION OF TRADE-OFFS BETWEEN SEXUAL AND ASEXUAL PHASES AND THE ROLE OF REPRODUCTIVE PLASTICITY IN THE GENETIC ARCHITECTURE OF APHID LIFE HISTORIES

Life‐history theory postulates that evolution is constrained by trade‐offs (i.e., negative genetic correlations) among traits that contribute to fitness. However, in organisms with complex life cycles, trade‐offs may drastically differ between phases, putatively leading to different evolutionary trajectories. Here, we tested this possibility by examining changes in life‐history traits in an aphid species that alternates asexual and sexual reproduction in its life cycle. The quantitative genetics of reproductive and dispersal traits was studied in 23 lineages (genotypes) of the bird cherry‐oat aphid Rhopalosiphum padi, during both the sexual and asexual phases, which were induced experimentally under specific environmental conditions. We found large and significant heritabilities (broad‐sense) for all traits and several negative genetic correlations between traits (trade‐offs), which are related to reproduction (i.e., numbers of the various sexual or asexual morphs) or dispersal (i.e., numbers of winged or wingless morphs). These results suggest that R. padi exhibits lineage specialization both in reproductive and dispersal strategies. In addition, we found important differences in the structure of genetic variance–covariance matrices ( G ) between phases. These differences were due to two large, negative genetic correlations detected during the asexual phase only: (1) between fecundity and age at maturity and (2) between the production of wingless and winged parthenogenetic females. We propose that this differential expression in genetic architecture results from a reallocation scheme during the asexual phase, when sexual morphs are not produced. We also found significant G × E interaction and nonsignificant genetic correlations across phases, indicating that genotypes could respond independently to selection in each phase. Our results reveal a rather unique situation in which the same population and even the same genotypes express different genetic (co)variation under different environmental conditions, driven by optimal resource allocation criteria.     

Genotypic variation among different phenotypes within aphid clones.

Most aphid species Hemiptera: Aphididae are parthenogenetic between periods of sexual reproduction. They are also highly polyphenic, with different adult morphs occurring in the life cycle, piz. winged, wingless, asexual and sexual. It is assumed that aphids born in a parthenogenetic clonal lineage are genetically identical regardless of the final adult form with the exception of sexual forms). Using the randomly amplified polymorphic DNA-polymerase chain reaction (RAPD-PCR) we have found that different asexual adult phenotypes winged and wingless of some clones of two cereal aphid species (the grain aphid, Sitobion avenae (F.) and the bird-cherry aphid. Rhopalosiphum padi (L.) may be distinguished by the presence or absence of one or more RAPD-PCR bands. In three of nine clones examined, such differences were found, and Southern blotting and hybridization of the discriminating bands confirmed these to be of aphid origin, rather than due to endosymbiotic bacteria or contaminating fungi. The main 248 and 296 bp bands, in the two species respectively, were sequenced and found to be A/T rich. The smaller band showed 57% homology with white striated muscle over a stretch of 90 bp. Genomic DNA treated with dimethyl sulphoxide to remove secondary structures still showed differences in RAPD-PCR profiles between winged and wingless morphs within the unusual clones. This discovery may be widespread and therefore it is important to understand the phenomenon in relation to clonal organisms.     

Short-term consequences of reproductive mode variation on the genetic architecture of energy metabolism and life-history traits in the pea aphid

Cyclically parthenogenetic animals such as aphids are able alternating sexual and asexual reproduction during its life cycle, and represent good models for studying short-term evolutionary consequences of sex. In aphids, different morphs, whether sexual or asexual, winged or wingless, are produced in response to specific environmental cues. The production of these morphs could imply a differential energy investment between the two reproductive phases (i.e., sexual and asexual), which can also be interpreted in terms of changes in genetic variation and/or trade-offs between the associated traits. In this study we compared the G-matrices of energy metabolism, life-history traits and morph production in 10 clonal lineages (genotypes) of the pea aphid, Acyrthosiphon pisum, during both sexual and asexual phases. The heritabilities (broad-sense) were significant for almost all traits in both phases; however the only significant genetic correlation we found was a positive correlation between resting metabolic rate and production of winged parthenogenetic females during the asexual phase. These results suggest the pea aphid shows some lineage specialization in terms of energy costs, but a higher specialization in the production of the different morphs (e.g., winged parthenogenetic females). Moreover, the production of winged females during the asexual phase appears to be more costly than wingless females. Finally, the structures of genetic variance-covariance matrices differed between both phases. These differences were mainly due to the correlation between resting metabolic rate and winged parthenogenetic females in the asexual phase. This structural difference would be indicating that energy allocation rules changes between phases, emphasizing the dispersion role of asexual morphs.     

Genetic variation in natural populations of the aphid Rhopalosiphum padi as revealed by maternally inherited markers

A survey on 148 clones of the aphid Rhopalosiphum padi from 11 widespread localities has been carried out to study the genetic structure of populations of this species as revealed by mitochondrial DNA restriction site and length polymorphisms as well as by restriction site analysis of a maternally inherited plasmid carried by the aphid eubacterial endosymbiont Buchnera aphidicola. Our results support the existence in the area under study of two main aphid maternal lineages strikingly coincidental with the two main reproductive categories displayed by this species. Those aphid clones possessing an incomplete life cycle that lacks the sexual phase (anholocyclic or androcyclic clones) show mitochondrial DNA (mtDNA) haplotype I and plasmid haplotype I, whereas those clones displaying the complete life cycle (holocyclic clones) posses some other distinct mtDNA haplotypes closely related to each other and plasmid haplotype II. While restriction-site analysis of maternally inherited markers points to a relatively ancient origin of anholocycly/androcycly (between 460 000 and 1 400 000 years) followed by interrupted gene flow with respect to the ancestral holocyclic population, mtDNA size variation also suggests that historical stochastic processes have a different effect on the evolution of both main aphid lineages. Evidence of occasional nuclear gene flow between lineages and its consequences on the correspondence between maternally inherited haplotypes and life cycle are also presented and discussed.     

Variability in the developmental parameters of bird cherry–oat aphid <Emphasis Type="Italic">Rhopalosiphum padi</Emphasis> (L.) (Homoptera,Aphididae) clones during the life cycle as a genotypic adaptation

The complexity of life cycles, clonal structure of populations, and polymorphism underpin the ability of aphids to quickly evolve adaptations and inflict greater damage to crops. Harmfulness of aphids can only be limited by controlling changes in the adaptive norm that occur during seasonal cycles. In this study, timing of emergence of the main morphs and their developmental traits as reflected in 27 parameters are established for 9 heteroecious holocyclic clones of the bird cherry–oat aphid Rhopalosiphum padi (Linnaeus, 1758). On the basis of ranking the clones by the performance index, 3 clones with good performance and 4 clones with bad performance were identified. Three intermediate clones were discovered, which are capable of prolonged anholocyclic development and of overwintering at the active stage. Omission of the generation that develops on the primary host may change the population dynamics and harmfulness of aphids on secondary hosts. It is shown that performance of clones should be assessed by using demographic characteristics of morph development and phenological and behavioral peculiarities. The work was carried out under field conditions and in outdoor metal grid cages.     

Association of aphid life stages using DNA sequences: A case study of tribe Eriosomatini (Hemiptera: Aphididae: Pemphiginae)

Association of aphid life stages based on a portion of COI sequence was applied in Eriosomatini. Three aphid specimens, nos. 17496, 19265a, and 19265b collected on Gramineae roots all clustered with Tetraneura chinensis Mordvilko with strong support. The average pairwise p‐distance among the four taxa was 0.001 (range, 0.000–0.002), and that among all the ingroup taxa was 0.065 (range, 0.000–0.141). This indicated that nos. 17496 and 19265 b were the secondary‐host morphs of T. chinensis. In this paper the secondary host morph of T. chinensis is described for the first time. With the identification of more species' secondary‐host morphs, aphids identification based on this morph will be made easily.     

Elimination of a specialised facultative symbiont does not affect the reproductive mode of its aphid host

Abstract.  1. Microorganisms that manipulate the reproduction of their hosts through diverse mechanisms including the induction of parthenogenesis are widespread among arthropods.
2. The pea aphid, Acyrthosiphon pisum , shows a variation in its reproductive mode, with lineages reproducing by cyclical parthenogenesis (obligate alternation of parthenogenetic and sexual generations each year) and others by obligate parthenogenesis (continuous asexual reproduction all year round). In addition, the pea aphid harbours, along with Buchnera the primary aphid endosymbiont, several facultative symbionts whose prevalence differs among host populations.
3. The possible influence of a Rickettsia facultative symbiont on the reproductive mode of its host was tested on two pea aphid clones by comparing the response of infected and uninfected individuals with the same genetic background to conditions that typically induce the production of sexual morphs.
4. No significant effect of the Rickettsia infection was found on the type of reproductive morphs produced (sexual vs. asexual) or on their quantities for the two clones.
5. However, the Rickettsia had a detrimental effect on the fitness of its aphid host, in apparent contradiction to the high prevalence of this symbiont in some host populations. It is suggested that this negative impact may disappear under specific environmental conditions, transforming a parasitic association into a mutualistic one.     

Inheritance of photoperiodic response in the bird cherry aphid, Rhopalosiphum padi

Abstract. The photoperiodic induction of presexual females (gynoparae) and males of the aphid Rhopalosiphum padi (L.) was examined in single clones collected from different latitudes (N clone from Blair Atholl, 56.5N 3.1W; C clone from Leeds, 53.5N 1.4W and S clone from Exeter, 50.4N 3.3W). Critical night lengths (CNLs) for gynopara and male production (CNLs: 50% of maximum production) and inter-clonal differences, defined by the different forms of progeny produced at a single discriminating night length (12 h 30 min), were measured at 16 ± 1C. The aphid clones differed in CNL and in the morphs produced at the discriminating night length. These differences were used to investigate the inheritance of the photoperiodic response. In crosses between clones the photoperiodic response showed considerable overall variation. The variation in CNLs indicated that the photoperiodic response was unlikely to affect the overwintering success after long-distance movement of clones from one latitude to another.     

Variation to cause host injury between Russian wheat aphid (Homoptera: Aphididae) clones virulent to Dn4 wheat

Biotypes are infraspecific classifications based on biological rather than morphological characteristics. Cereal aphids are managed primarily by host plant resistance, and they often develop biotypes that injure or kill previously resistant plants. Although molecular genetic variation within aphid biotypes has been well documented, little is known about phenotypic variation, especially virulence or the biotype's ability to cause injury to cultivars with specific resistance genes. Five clones (single maternal lineages) of Russian wheat aphid, Diuraphis noxia (Kurdjumov) (Homoptera: Aphididae), determined to be injurious to wheat, Triticum aestivum L., with the Dn4 gene, were evaluated on resistant and susceptible wheat and barley, Hordeum vulgare L., for their ability to cause chlorosis, reduction in plant height, and reduction in shoot dry weight. Variation to cause injury on resistant 'Halt' wheat, susceptible 'Jagger' wheat, and resistant 'STARS-9301B' barley was found among the Dn4 virulent clones. One clone caused up to 30.0 and 59.5% more reduction in plant height and shoot dry weight, respectively, on resistant Halt than other clones. It also caused up to 29.9 and 55.5% more reduction in plant height and shoot dry weight, respectively, on susceptible Jagger wheat. Although STARS-9301B barley exhibited an equal resistant response to feeding by all five clones based on chlorosis, two clones caused approximately 20% more reduction in plant height and shoot dry weight than three other clones. The most injurious clones on wheat were not the most injurious clones on barley. This is the first report of variation to cause varying degrees of plant damage within an aphid biotype virulent to a single host resistance gene. A single aphid clone may not accurately represent the true virulent nature of a biotype population in the field.     

Variation in clonal diversity in glasshouse infestations of the aphid, Aphis gossypii Glover in southern France

Aphis gossypii is an aphid species that is found throughout the world and is extremely polyphagous. It is considered a major pest of cotton and cucurbit species. In Europe, A. gossypii is assumed to reproduce exclusively by apomictic parthenogenesis. The present study investigates the genetic diversity of A. gossypii in a microgeographic, fragmented habitat consisting of eight glasshouses of cucurbit crops. This analysis, which was based on the results from seven microsatellite loci, has confirmed that A. gossypii populations in southern France are primarily asexual, as only 12 nonrecombinant genotypic classes (clones) were identified from 694 aphids. Moreover, a high proportion of the aphids (87%) had one of three common genotypes. No significant correlation was found between genotypic class and host plant species. Within a glasshouse population of A. gossypii, a significant reduction in clonal diversity was observed as the spring/summer season progressed. The final predominance of a clone could result from interclonal competition. At the microgeographic level (i.e. glasshouses within a 500-m radius), significant genetic subdivision was detected and could be attributed to founder effects and the limitation of gene flow imposed by the enclosed nature of the glasshouse structure. Finally, the three common clones of A. gossypii detected in 1996 reappeared in spring 1997 following the winter extinction, together with rare clones that had not previously been seen. The probability that A. gossypii overwinters within refuges at a microgeographic scale from which populations are renewed each spring is discussed.     

High variation in host adaptation among clones of the pea aphid,Acyrthosiphon pisum on peas,Pisum sativum

The performance of one clone of the pea aphid,Acyrthosiphon pisum (Harris), was assessed on 37 different cultivars and species ofPisum L. In addition, random samples of 36 pea aphid clones collected on alfalfa and clover were tested on a selection of fivePisum sativum L. cultivars. Aphid performance was evaluated in terms of the mean relative growth rate (MRGR) during the first five days of life or other life history variables. The MRGR of the first-mentioned pea aphid clone differed little between cultivars. No significant differences in MRGR were found between wild and cultivatedPisum species or between modern and oldP. sativum cultivars. There was considerable variation in host adaptation among the 36 pea aphid clones within each sampled field. The pea aphid clones showed no consistent pattern in performance on four of the five pea cultivars i.e. there was a significant pea aphid genotype —pea genotype interaction. On one of the cultivars all clones performed well. Pea aphid clones collected from red clover generally performed relatively poorly on pea cultivars, in contrast to the pea aphid clones collected on alfalfa. There was no difference in performance between the two pea aphid colour forms tested. Possible reasons for the high variation and the observed adaptation patterns are discussed. The fact that all clones were collected in two adjacent fields indicates thatA. pisum shows high local intraspecific variability in terms of host adaptation.     

Competition and dispersal in the pea aphid: clonal variation and correlations across traits

Abstract.  1. The presence of an across-species trade-off between dispersal ability and competitive ability has been proposed as a mechanism that facilitates coexistence. It is not clear if a similar trade-off exists within species. Such a trade-off would constrain the evolution of either trait and, given appropriate selection pressures, promote local adaptation in these traits.
2. This study found substantial levels of heritable variation in competitive ability of the pea aphid, Acyrthosiphon pisum Harris (Homoptera: Aphididae), measured in terms of relative survival when reared with a single clone of the vetch aphid, Megoura viciae Buckton (Homoptera: Aphididae).
3. Pea aphids can move to new patches by either flying (longer distance dispersal) or walking (local dispersal) from plant to plant. There was considerable clonal variation in dispersal ability, measured in terms of the proportion of winged offspring produced, and ability to survive away from their host plant.
4. Winged individuals showed longer off-plant survival times than wingless forms of the same pea aphid clone.
5. There was no evidence of a relationship between clonal competitive ability and either measure of dispersal ability, although the power of the test is limited by the number of pea aphid clones used in the trial.
6. However, there was a positive correlation between clonal fecundity and the proportion of winged offspring produced. Although speculative, it is suggested that clones that are more likely to either overwhelm their host plant or attract higher numbers of natural enemies as a result of having higher fecundity are more likely to produce winged morphs.     

Effect of light intensity on colour morph formation and performance of the grain aphid Sitobion avenae F. (Homoptera: Aphididae)

The grain aphid Sitobion avenae F., one of the major pest aphids of cereals in Central Europe, exhibits colour polymorphism, even within the same clones. Although there is evidence that green and brown morphs of S. avenae contain different carotenoids, the mechanisms determining the induction of colour morphs are unknown. The common understanding is that the formation of colour morphs is controlled by light and affected by genetic and environmental factors and by host plant species. So far, there is no unequivocal evidence that light intensity, photoperiod, or a mixture of several variables are involved in the induction of S. avenae colour formation, resulting in the induction of S. avenae colour formation and carotenoid synthesis.Here we determined the effect of light intensity on the colour formation and performance of ten clones of S. avenae with experiments that controlled for the effects of host plant and genetic factors. We found that some clones remained green under all test conditions. In other clones, colour morph formation was controlled by light. The synthesis of carotenoids correlated with changes in colour formation. Host plant did not affect colour formation in the ten clones studied. Although colour of the aphid clones did not affect their performance, high light intensity increased the fecundity and fresh weight of S. avenae clones, while low light intensity stimulated the production of alatae.     

A geographic mosaic of trophic interactions and selection: trees, aphids and birds

Genetic variation in plants is known to influence arthropod assemblages and species interactions. However, these influences may be contingent upon local environmental conditions. Here, we examine how plant genotype-based trophic interactions and patterns of natural selection change across environments. Studying the cottonwood tree, Populus angustifolia, the galling aphid, Pemphigus betae and its avian predators, we used three common gardens across an environmental gradient to examine the effects of plant genotype on gall abundance, gall size, aphid fecundity and predation rate on galls. Three patterns emerged: (i) plant genotype explained variation in gall abundance and predation, (ii) G×E explained variation in aphid fecundity, and environment explained variation in gall abundance and gall size, (iii) natural selection on gall size changed from directional to stabilizing across environments.