Temporal changes in host adaptation in the pea aphid, Acyrthosiphon pisum

Ecological Entomology ( 1996) 21,56-62 Temporal changes in host adaptation in the pea aphid, Acyrthosiphon pisum J N A S S A N D S T R M Sweden Department of Entomology, Swedish University of Agricultural Sciences. UppsaIa, Abstract. 1. Temporal changes in host adaptation were followed in a local population of the pea aphid, Acyrrhosiphon pisum. Aphid clones were collected in one alfalfa and one clover field at three different times. In the spring, first-generation females were collected. Later, in the autumn, females belonging to the last parthenogenetic generation were collected. Lastly, sexual females were collected after mating in autumn and allowed to produce eggs which were hatched. The performance was evaluated on alfalfa and clover. The spring-collected individuals were also assessed on peas. 2. On the overwintering hosts clover and alfalfa, the clones performed best on the plant of origin, i.e. negative correlations in performance. Correlations between performance on the temporary summer host, pea, and that on clover/alfalfa were weak or nonsignificant. 3. Significant variation in host performance was found within both host fields at spring, which is a prerequisite for changes in clone composition due to selectiodmigration. 4. The clones from alfalfa showed an increase in mean performance on alfalfa between spring and autumn, whereas no changes among the clones from the clover field were observed. This difference in seasonal response between the two fields could have been the result of larger variation in performance among the alfalfa clones andor a differential tendency to migrate among clones in both fields. 5. After sexual recombination in the autumn, mean performance in the alfalfa field returned to the spring level, probably as a result of emergence of new genetic combinations. In the clover field, mean performance did not change significantly over time. Key words. Acyrthosiphon pisum, pea aphid, host plant adaptation, temporal change, genetic variation. Introduction Host plant aftiliation seems to be more dynamic in some herbivorous insect species than in others. There are several examples of rapid adaptation to resistant crop cultivars in 'pest' insects, especially aphids. Alterations in oviposition choice and/or host utilization have been recorded in artificial selection experiments after only eleven to sixteen generations (Gould. 1979; Wasserman & Futuyma, 1981). One fundamental prerequisite for potential host changes is genetic variability in host utilization. Such variability has been found in several phytophagous insect species (Futuyma & Peterson, 1985). including parthenogenetic aphids (Gould, 1983). However, most studies have been concerned with large-scale variation. Fewer studies have documented variation within a local geographic area. Weber (1985), Via (1991a) and Correspondence: Dr Jonas Sandswm. Swedish University of Agricultural Sciences Department of Entomology, P.O. Box 744. S-75 7 Uppsala. Sweden. Sandstriim (l994a) have carried out such studies on aphids. It is the genetic variation present within a local population that is most relevant for immediate adaptive responses (Futuyma & Philippi. 1987), e.g. for adaption to a resistant crop cultivar. Although there is overwhelming evidence for genetic variation in pea aphid (Acyrthosiphon pisum Harris) (Homoptera: Aphididae) host-use characteristics, much of the data regarding aphid clones are based on studies where aphids were drawn from more than one interbreeding population (Pilson, 1992). However, Via (1991a) collected pea aphid clones in two different crop fields, alfalfa and clover, within a local area and found significant variation in aphid performance within each field, which was probably of genetic origin (Via, 1991 b). The pea aphid population also showed local adaptation to each host (Via, 1991a). Via (1991a) argued that this pattern of variance in fitness within each crop field would make further evolution within fields possible, especially in newly c olonized fields, and that this could lead to enhanced local adaptation and increased specialization. 56 8 1996 Blackwell Science Ltd

Temporal changes in host adaptation in the pea aphid 57 To learn more about the evolutionary capacity of the pea aphid I examined seasonal changes in host adaptation within a local population. In Sweden, the pea aphid's life cycle is cyclical parthenogenetic with one sexual generation in the autumn and several parthenogenetic generations during the summer. In spring, parthenogenetic females, also called fundatrices, hatch from sexually produced eggs. Genetic variation should be at its peak around this time because new genetic combinations will be exposed after the sexual recombination which occurred during the preceding autumn. Each fundatrix gives rise to a clonal lineage of parthenogenetic females that reproduce for five to ten generations (Markkula, 1963). Variation in performance among these clones will lead to the proliferation of clones with higher performance. Thus, if there is selection among clones with varying host-plant performance, mean performance should increase and variation should gradually decline with succeeding parthenogenetic summer generations. This pattern of temporal change could be counterbalanced or enchanced by the migration of winged parthenogenetic females to and/or away from the fields. Thus, I expected to find a temporal pattern of variation in performance within each field that is influenced by the alternating parthenogenetic and sexual generations. To follow such patterns, performance of pea aphid clones from newly colonized alfalfa and clover fields was assessed at three different times during one yearfife cycle. Newly colonized fields were chosen because variation should be large, and consequently temporal changes should be easy to detect. Material and Methods Study area and aphids. The pea aphid, Acyrthosiphon pisum (Harris), is oligophagous, feeding on several leguminous plant species. In the study area, Uppsala, Sweden, the main food plants for pea aphids are the crops alfalfa, red clover and peas. These crops constitute only a minor part of the agricultural landscape which is dominated by cereals. Wild leguminous host plants in the surroundings are probably of minor importance for the pea aphids in the study area because plant density is low compared with the cultivated host plants. The two main perennial hosts used for overwintering, alfalfa and red clover, are often planted in mixed fields or, in this case, in pure stands for a period of 3-5 years. The annual crop, peas, is only a temporary summer host which is planted in pure stands. The whole life cycle of pea aphids can be completed on the perennial hosts without migration to pea. Pea aphids in Sweden occur in a green and a red colour morph, both of which are present in the study area. Since these colour morphs are stable in clonal lineages and the red morph dominates in crosses it was concluded that they are genetically determined (Miiller, 1971). Pea aphids for the experiments were collected in one alfalfa field (9.5 ha) and one adjacent red clover field (8.5 ha) in 1992 at Uppsala, Sweden. Both fields were sown and colonized by pea aphids in the preceding year, 1991. Aphids were sampled at three different times. First, in May, adult fundatrices, first-generation aphids hatched from eggs earlier the same spring, were collected. Next, in early September females belonging to the last parthenogenetic generation of the season were collected. Finally, at the end of September, mated, sexual females were collected. Aphids were collected by sweepnetting at random in each field at sites that were widely spaced to avoid collecting aphids from the same clone. After each sampling occasion, fifteen clones of pea aphids from each field remained after parasitized and fungal-diseased aphids were removed (only thirteen clones remained from clover at autumn). Descendants of the aphids in the first and second samplings, designated as spring and autumn generations respectively, were propagated under parthenogenetic conditions on broad bean until mid-october when the first trial was performed. The sexual females from the third sampling, the overwintering generation, were allowed to produce eggs which were overwintered under natural conditions outdoors. At the end of the winter the eggs were taken indoors and allowed to hatch. From each brood, the offspring from one randomly chosen egg was propagated under parthenogenetic conditions on broad bean for three generations, after which the second trial was started. Aphid stock cultures were kept in cages in glasshouse at a temperature of at least 18"C, with a minimum photoperiod of 17 h daylight supplemented with artificial light when needed (Philips HPI-T, 4 W). All clones were reared on broad beans (Vicia faba L., cv. Major), on which they performed well as indicated by their high adult weight. No clones were lost during propagation. Experiments. All pea aphid clones were tested on alfalfa (Medicago sativa L. cv. Sverre) and red clover (Trifolium pratense L. cv. Hermes 11). In addition, the clones from the first spring generation were also tested on peas (Pisutn sativum L. cv. Vreta) (Sandstriim, 1994a). Plants were cultivated under the same environmental conditions as the aphids. All test plants were grown in 13-cm-diameter plastic pots in soil (P-jord, Hasselfors garden, Hasselfors, Sweden). The plants were watered with fertilized water once a day. The experiments were performed in a glasshouse at 2 f 1 C. 7 f 1% r.h. and a photoperiod of at least 17 h daylight supplemented with artificial light as described above. Pea plants used were 16 days old at the beginning of the experiment, and the alfalfa and red clover plants were about 4-5 days old. In the first trial descendants from the spring and autumn generation pea aphids were used. Each plant-pea aphid clone combination was tested twice using two replicates. The full experimental design was 2 plant species x 2 aphid origins x 15 pea aphid clones per origin x 2 collection times x 2 blocks x 2 replicates. Performance on peas was tested in a separate trial (Sandstrom, 1994a). In the second trial, descendants from the overwintering generation were used. Each plant-pea aphid clone combination was tested twice using two replicates. The full experimental design was 2 plant species x 2 aphid origins x 15 pea aphid clones per origin x 2 blocks x replicates. Since the first and second trial were made separately comparisons between the spring and autumn generations are more reliable than comparisons between the overwintering generation and the two other generations. In each replicate two apterous females at the beginning of their reproductive period were placed on one plant. The females had free access to the whole plant, but were prevented from leaving it by a perforated plastic bag, Cryovac (W. R. Grace Ltd, Cambridge, England). After 6 h the females were removed, and five to ten nymphs were left on each plant. Afterwards the plants were inspected every 12 h. Once the aphids had started to reproduce 1996 Blackwell Science Ltd, Ecologicd Entomology 21: 56-62

58 Jonas Sandsrriim the experiment was terminated. Survival during the nymphal stages and the time elapsed from birth to the onset of reproduction of the survivors (age at first reproduction) were recorded. Slurisricol unul.vses. The results were analysed using the SAS software package (SAS institute. Cary. N.C., U.S.A.). Life history variables in the first and second experiments were analysed using the GLM and REG procedures (SAS Institute Inc.. 1985). Age at first reproduction and mortality data were analysed in a mixed model with nested factors using the GLM procedure. Means were compared using Tukey's test. The variable 'nymphal mortality' was arcsin transformed prior to statistical analysis to achieve normality. Since the factor 'block' had no significant effect in the analysis of variance, it was omitted to simplify the models. Pea aphids were sampled from only one field of alfalfa and clover. This means that the results from the statistical analysis not necessarily reflects general differences between aphid clones from alfalfa and clover, it could also include differences between individual fields. Results A nonsignificant correlation in performance, measured as age at first reproduction and nymphal mortality, was found for springcollected pea aphid clones on alfalfa and on peas. Similarly, the correlation was weak or non-significant for aphids on red clover and on peas (Table I, Fig. I ), even if the aphid clones from the two origins were tested separately. Strong negative correlations in both variables were found between performance on alfalfa and on red clover for pea aphid clones from all three collection times (Table I. Fig. 2). All clones showed relatively good performance on the host from which they had been collected, but very few clones could survive long on both alfalfa and clover. Clones whose age at first reproduction exceeded 1 I days showed very poor performance and did not survive for more than a few generations. The data presented in Fig. 2 were subjected to two separate analyses of variance, one for age at first reproduction on the same plant species that the clones had been collected on, i.e. the plant of origin, and one for age at first reproduction on the non-origin plant (Table 2). Although both tests yielded consistent results. significance levels were lower on the non-origin plant. partly owing to higher variation and the loss of several replicates due to high nymphal mortality. The effect of 'aphid origin' was nonsignificant. indicating that the performance of clones collected 8 1 12 14 B # I a - 88 $ 8 1 12 14 Age at first reproduction on pea Flg. 1. Relationship between performance on pea and that on (A) alfalfa and (B) red clover, respectively, for the thirty pea aphid clones collected in spring. Performance evaluated as age at first reproduction (days)., Clones collected on alfalfa; A. clones collected on red clover. on alfalfa was equal to that of clones collected on clover when tested on their plant of origin (P =.1898) and equally poorly on a non-origin plant (P =.59). The effect of 'time' was significant in both tests, indicating that mean performance differed between sampling times (P =.1 7 and P =.43 respectively). The interaction 'aphid origin x time' was significant on both plant of origin (P =.ooi) and non-origin plant (P =.ool). This interaction is illustrated in Fig. 3. On the plant of origin Table 1. Correlations between pea aphid performance on different host plants at different collection times. Performance was measured as age at first reproduction and mortality during the nymphal stages. Analysis of linear regressions. Host plant combination Age at first reproduction Nymphal mortality n slope P n slope P Spring Autumn Winter A I fa1 fa-pea Clover-pea Alfalfa-clover Alfalfa4over Alfalfa-clover 3.43.985 3 -.469.257 3 -.698 O.ooO1 25 -.657 O.ooO1 29-1.4 O.ooO1 3.%2.895 3 -.916.787 3 -.778.1 28 -.845 O.ooO1 3 -.82.1 1996 Blackwell Science Ltd. Ecological Entomology 21: 56-62

14 12 - - C c 12-1 3 l o- I A A % AA A A A A 4% n A: Spring I 8 1 12 14 = m 141 & 6: Autumn i n 12...9.. @ C: Winter 8 1 12 14 Age at first reproduction on clover (days) Flg. 2. Performance on red clover versus performance on alfalfa for pea aphid clones collected at three different times: (A) first-generation aphids from spring, (B) last-generation aphids from autumn and (C) aphid generation hatched from overwintering eggs. Performance evaluated as age at first reproduction (days)., Clones collected on alfalfa; A, clones collected on red clover. Temporal changes in host adaptation in the pea aphid 59 (Fig. 3A), the mean age at first reproduction of the clones collected on alfalfa decreased between spring and autumn, but increased back to springtime levels between autumn and winter. Temporal changes in the mean age at first reproduction of the clones collected on clover showed a pattern similar to that found with the alfalfa clones but much less pronounced. On the nonorigin plant (Fig. 3B) the mean age at first reproduction of the clones collected on alfalfa did not change significantly between collection times. The mean age at first reproduction of the clones collected on clover did not change significantly between spring and autumn but showed a significant decrease between autumn and winter. Analysis of variance of the second performance variable, nymphal mortality gave similar results, but significance levels were lower (Table 3). The analysis of nymphal mortality on the plant of origin was non-significant because nymphal mortality was very low for all aphid clones. The analysis of nymphal mortality on the non-origin plant revealed only time as a significant effect (P =.254). To see if each field contained significant variation in host performance at spring, performance on the plant of origin in each field was analysed separately. The first performance variable, age at first reproduction, showed significant variation for aphid clones originating from alfalfa (df = 14, F = 3.67, P =.4) and for aphid clones originating from clover (df = 14, F = 2., P =.397). The nymphal mortality was close to zero in both fields so no significant variation could be detected in this variable among the aphid clones in each field. In late autumn production of sexual morph was induced in all pea aphid clones collected at spring and autumn. All clones produced exclusively unwinged males and females. Frequencies of the two colour morphs differed between fields. In the alfalfa field the green morph dominated (c. 8%), whereas the red morph dominated (c. 65%) in the clover field (Table 4). This pattern did not change much over time. The performance variable age at first reproduction was subjected to a separate analyses of variance including the factor colour morph. This analysis did not reveal any significant factors with colour morph involved, indicating that neither of the morphs differed in their performance between alfalfa and clover. Table 2. Results of analysis of variance of age at first reproduction (days) on the plant of origin, i.e. the same plant as the pea aphid clones had been collected on, and on the non-origin plant. Plant of origin Non-origin plant Source of variation d.f. S.S. F-ratio P d.f. S.S. F-ratio P Model 87 66.5 4.51 O.OOO1 83 24.4 3.39 O.OOO1 Aphid origin I 1.1 1.75.1898 I 8. 3.93.59 Time 2 8.8 6.88.17 2 13.6 3.35.43 Aphid origin x Time 2 4.6 3.57.327 2 13.3 3.26.435 Aphid clone (Aphid origin, Time) 82 52.8 3.8 O.OOO1 78 159. 2.8 O.OOO1 Error 264 44.7 58 42.2 Total 351 111.3 141 246.5 1996 Blackwell Science Ltd, Ecological Entomology 21: 56-62

6 Jonas Sandstrom a t?! "t A Plant of oriain Spring Autumn Winter B Non-origin plant Spring Autumn Winter Time Fig. 3. Means of age at first reproduction for pea aphid clones collected at three different times. Figure A shows performance on the plant of origin, i.e. the plant species they were collected on. and figure B shows performance on the non-origin plant. Clones from alfalfa are represented by and those from red clover by A. Markers and lines m least-squares means with standard errors. Discussion In this study I tested the performance of pea aphid clones on the perennial legumes alfalfa and clover, which both are overwintering hosts. I also included a temporary, annual summer host, pea, in my test. On clover and alfalfa the aphids performed best on the plant from which they had originally been collected, i.e. strong negative correlations in performance in accordance with Via (1991a). The negative correlation suggests that there is a cost involved in being simultaneously adapted to both alfalfa and clover. Physiological trade-offs concerning the neutralization of plant toxins or utilization of nutrients, etc.. are the most probable source of such costs. However, no correlation between performance and host nitrogen quality (amino acid composition) was found in a previous study (Sandstram. 1994b). Weak or no correlations were found between performance on the perennial hosts and the annual host plant pea. This raises the question of whether the closer and more prolonged association with the overwintering hosts could result in certain selective factors that might constrain adaptation to both hosts at the same time. Negative genetic correlations of performance on different host plants has been one of the major potential explanations for evolution of host specialization in phytophagous insects (Futuyma & Philippi, 1987). Although clear examples of negative correlations, or 'trade-offs', within populations have often been sought they have only rarely been found (Via, 1991a). Performance on pea tended to be better for pea aphid clones from alfalfa than for clones from clover (see also Sandstram. 1994a). An explanation of this difference may be that adaptation to alfalfa is accompanied by a larger variability in host use, giving alfalfa clones an advantage over clover clones when it comes to colonizing pea plants from overwintering hosts every spring. Alfalfa clones (green morphs) also showed a stronger tendency to produce winged morphs during spring (Bommarco & Ekbom, 1996.) which might reflect another adaption to pea utilization. Temporal changes in age at first reproduction on the host of origin were found within the alfalfa field; the mean age on alfalfa decreased from spring to autumn, whereas no change was observed in the clover field. These results suggest that a change in clone composition had taken place in the alfalfa field. There are two plausible, non-mutually exclusive explanations for this: (I) Improved performance in the alfalfa field could have been the result of selection during the parthenogenetic generations, i.e. clonal selection. If such selection occurred why did not it not occur in the clover field as well? Variability in age at first reproduction in the spring was lower in the clover field; thus low variability could have constrained selection in the clover field. Table 3. Results of analysis of variance of nymphal mortality on the 'plant of origin', i.e. the same plant as the pea aphid clones had been collected on, and on the 'non-origin plant'. Plant of origin Non-origin plant Source of variation d.f. S.S. F-ratio P d.f. S.S. F-ratio P Model 81.527.86.7956 87 3.2 1.39.25 Aphid origin I.16 2.64.183 I.57 1.73.1926 Time 2.5.38.6842 2 2.52 3.84.254 Aphid origin x Time 2.1.1.972 2.9.14.8677 Aphid clone (Aphid origin, Time) 82.54.87.765 82 26.9 1.32.554 Error 264 1.863 264 65.93 Total 351 2.39 351 96.13 1996 Blackwell Science Ltd, Ecological Enromo/ogy 21: 56-62

Temporal changes in host adaptation in the pea aphid 6 1 Table 4. Frequencies of the red and green morphs of the pea aphid in the two test fields at different collection times. Results from all clones collected, including clones not used for performance tests. The colour of the clones collected at winter refers to the offspring of the fundatrices hatched from eggs. Alfalfa field Clover field Collection time n Green Red n Green Red Spring Autumn Winter 48 75% 25% 62 84% 16% 2 85% 15% 41 37% 63% 48 27% 73% 18 33% 67% Selection for higher performance in the clover field could also been masked or counterbalanced by other factors, e.g. colonization by clones with lower performance. (2) Differences between the two fields could also have been a result of differential migration away from the fields. This implies that the tendency to migrate, i.e. to produce winged morphs, varies among clones and is coupled to host utilization. The fundatrices and the next following aphid generations in spring, show very large variation with regard to alate production (Lamb & MacKay, 1979; Bommarco & Ekbom, 1996.). Low host quality induces alate production in pea aphids (Sutherland, 1969). Thus, clones performing poorly on alfalfa, presumably because it does not offer them a high quality source of food, might have a higher tendency to migrate, which would enhance the mean performance of the remaining clones. The absence of any change in performance in the clover field could be explained by a lower migratory tendency of red colour morph (Markkula, 1963; Bommarco & Ekbom, 1996) which dominates in clover. Mean age at first reproduction on the host of origin between autumn and winter increased back to spring levels in the alfalfa field, but remained unchanged in the clover field. The increase in alfalfa was probably a result of sexual recombination in autumn; i.e. new genetic combinations will arise, resulting in an increased variation in performance as well as lower mean performance in the overwintering generation (offspring of sexuals). Few other examples of temporal changes in host specialization have been reported. The peach aphid, Myzus persicae, exhibits local host adaptations to different crops (Weber, 1985). Weber (1986) contended that this species should also show temporal changes in performance, but failed to find any. However, there was a short period between samplings (6 weeks), the hosts were annusl and the adaptations were less distinct compared to those observed in this study. Rhomberg et al. (1989, who studied temporal changes in different enzyme and colour morph loci in the rose aphid, Macrosiphum rosae, found that there was a considerable amount of seasonal change. One of the enzyme loci went through a regular seasonal cycle of alterations, perhaps as a result of clonal selection and migration. The relations between these loci and performance on the host were unknown. The two fields in this study had been sown and colonized by pea aphids during the year before the first spring collection. Pea aphid clones collected that spring were highly specialized in both fields studied. If the correlation between performance and host preference was weak in colonizing aphids, one would expect host use to be less specialized in spring. The pattern found suggests that alfalfa-adapted clones colonized alfalfa and that clover-adapted clones colonized clover. Results from laboratory tests with winged individuals from the spring and autumn samplings indicate that host performance is correlated to host selection because these aphids very rarely deposited nymphs on the wrong plant even when they landed on it; instead they took off again within a few hours (umpublished data). Because of the strong negative correlation between performance on alfalfa and that on clover, one should expect the temporal pattern also to be shown on the non-origin host, but in the opposite direction. This was nearly true, but the clones collected on alfalfa, which showed clear differences on the plant of origin, showed less distinct differences on the non-origin plant and vice versa for clones collected on clover (Fig. 3B). This discrepancy can be explained as follows. First, performance on the nonorigin plant was generally very low. Because performance is on the border of survival the variation is larger and consequently more than half of the replicates were lost. Second, the negative correlation between alfalfa and red clover is nonlinear, the curve being L-shaped. Consequently, it is hard to predict how performance on the non-origin host will vary in response to small changes in performance on the host of origin. Although the frequencies of the two coloured morphs differed greatly between fields, this variation was not due to any differences in host performance between the colour morphs; i.e. they did not differ in performance on alfalfa or clover. The variation in frequencies might be due to some other selective force that differs between fields, or it might be a result of genetic drift if pea aphids from alfalfa and clover are genetically isolated. The relative proportions of the two morphs in the fields remained rather stable between sampling occasions. All clones collected in the spring and autumn in this study produced unwinged males only. Sexual females of pea aphids are always apterous, whereas males can be either apterous or, more rarely, winged (Markkula, 1963). The unwinged sexual morphs are restricted in their movements which can lead to assortive mating, i.e. mating among individuals adapted to the same host or of the same clone. Assortive mating can be an advantage for the pea aphid, since it would prevent clones adapted to alfalfa from mating with clover-adapted clones. The offspring of such matings would probably perform poorly on both plants. Assortive mating will also reduce gene flow and should therefore help to maintain the high intraspecific variability (Ward, 1991) found in the pea aphid in the studied fields. In this study, I have tried to shed light on temporal and spatial patterns of host utilization within a pea aphid population. This population shows large variability in host performance, but shows only limited temporal changes in host associations. Q 1996 Blackwell Science Ltd, Ecological Entomology 21: 56-62

62 Jonas Sandstrom Ac knowlodgments B. Ekbom. S. Larsson and J. Pettersson offered helpful comments on the manuscript. D. Tilles improved the English. I would also like to thank S. Via for inspiration through her articles. All of the above persons are gratefully acknowledged. This study was partly supported by a grant from the Swedish Council for Forestry and Agricultural Research. References Bommarco. R. & Ekbom. B. (1996) Variation in pea aphid population development in three different habitats. (In preparation.) Futuyma. D.J. & Peterson, S.C. (1985) Genetic variation in the use of resources by insects. Annual Review of Entomology. 3. 2 17-238. Futuyma. D.J. & Philippi. T.E. (1987) Genetic variation and covariation in responses to host plants by Alsophila pomcraria (Lepidoptera: Geomeuidae). Evolurion, 41,269-279. Gould, F. ( 1979) Rapid host range evolotion in a population of the phytophagous mite Tetranychus urticae Koch. Evolurion. 33, 79 1-82. Gould, F. (1983) Genetics of plant-herbivore systems: Interactions between applied and basic study. Variable Plants and Herbivore in Natural and Managed Systems (ed. by R. F. Denno and M. S. McClure), pp. 599-653. Academic Ress, New York. Lamb. R.J. & MacKay. P.A. (1979) Variability in migratory tendency within and among natural populations of pea aphid, Acyrthosiphon pisum. Oecologia (Berlin), 39, 289-299. Markkula. M. ( 1963) Studies on the pea aphid, Acyrthosiphon pisum Harris (Horn., Aphididae), with special reference to the differences in the biology of the green and red forms. Annales Agricultume Fenniae, 2. 1-3. Miiller. F.P. ( 197 I) Isolationsmechanismen zwischen sympatrichen bionomichen Rassen am Beispiel der Erbsenblattlaus Acyrrhosiphon pisum (Harris)(Homoptera. Aphididae). Zuologische Jahrbuch Sysremarics. 98. 131-152. Pilson. D. (1992) Insect distribution patterns and the evolution of host use. Plant Resistance to Herbivores and Pathogens: Ecology. Evolurion. and Generics (4. by R. S. Fritz and E. L. Simms). pp. 12-139. University of Chicago Ress. Rhomberg, L.R.. Joseph. S. & Singh, R.S. (1985) Seasonal variation and clonal selection in cyclically panhenogenetic rose aphids (Macrosiphum rosae). Canadian Journal of Generics and Cytolo~y. 27.224232. Sandstrt)m. J. (1994a) High variation in host plant adaptation among clones of the pea aphid, Acyrrhosiphon pisum on peas. Pisum sativum. Enromologia Experimenralis el Applicata. 71. 245-256. SandsWm. J. (1994b) Performance of pea aphid (Acyrthosiphon pisum) clones on host plants and synthetic diets mimicking the same plants phloem amino acid composition. Journal of Insect Physiology. 4. 151-157. SAS lnstitute Inc. (1985) SAP User s Guide: Sraristics. Version 5 Edition. SAS lnstitute Inc.. Cary. N.C. Sutherland, O.R.W. (1969) The role of the host plant in the production of winged forms by two strains of the pea aphid. Acyrrhosiphon pisum. Journal of Insect Physiology. IS. 21 79-221. Via. S. (1991a)The genetic structure of host plant adaptation in a spatial patchwork Demographic variability among reciprocally transplanted pea aphid clones. Evoloution, 45.827-852. Via. S. (1991b) Specialized host plant performance of pea aphid clones is not altered by experience. Ecology, 72. 142-1427. Ward, S.A. (1991) Reproduction and host selection by aphids: the importance of rendezvous hosts. Reproducrive Behaviour of Insects: Individualsandhpuhrions (4. by W. J. Bailey and J. Ridsdill-Smith), pp. 22-226. Chapman & Hall, London. Wasseman. S.S. & Futuyma. D.J. (1981) Evolution of host plant utilization in laboratory populations of the southern cowpea weevil. Callosobruchus maculatus Fabricius (Coleoptera: Bruchidae). Evolurion. 34,65417. Weber, G. (1985) Genetic variability in host plant adaptation of the green peach aphid. Myzus persicae. Enromologia Experimenralis et Applicara. 1.49-56. Weber. G. (1986) Ecological genetics of host plant exploitation in the green peach aphid. Myzus persicae. Entomologia Experimentalis el Applicara, 4, 161-168. Accepted 24 July 1995 1996 Blackwell Science Ltd, Ecological Enromo1og.v 21: 56-62