ISOLATING A ROLE FOR NATURAL SELECTION IN SPECIATION: HOST ADAPTATION AND SEXUAL ISOLATION IN NEOCHLAMISUS BEBBIANAE LEAF BEETLES

Muller (1942) and Mayr (1963) hypothesized that natural selection indirectly causes the evolution of reproductive barriers between allopatric populations by causing adaptive genetic divergence that pleiotropically promotes prezygotic or postzygotic incompatibility. Under this mechanism, herbivorous insect populations should be more prone to speciate if they are adapting to different host plants, because the evolution of reproductive isolation will be accelerated above the rate promoted by genetic drift and host-independent sources of selection alone. Although the Muller-Mayr hypothesis is widely accepted, little direct evidence has been collected in support of selection's role in allopatric speciation. This paper offers a method for isolating and evaluating the contribution of host plant-related natural selection pressures to the reproductive isolation between allopatric herbivore populations. The host-related selection hypothesis (HRSH) predicts that herbivore populations using different host plants should be more reproductively isolated than those using the same host, other things being equal. Here, I test this hypothesis using Neochlamisus bebbianae, an oligophagous leaf beetle with a geographically variable host range. In each of two sets of experiments (contrast I, contrast II), I compared two beetle populations (Georgia and New York) that use the same host (Acer) in nature and a third population that natively uses a different host (Betula in Oklahoma [CI], Salix in Ontario [CII]). Experiments showed that “different-host” populations were more strongly differentiated in host-use traits (oviposition, host fidelity, feeding response, larval performance) than were “same-host” populations and that each population most readily uses foliage from its native host. As predicted by the HRSH, sexual isolation was also greater between the adaptively divergent different-host populations (from Betula vs. Acer, from Salix vs. Acer) than between the same-host populations (from Acer), which were undifferentiated in host-use traits. Interpreting these results in a historical context provided by mtDNA sequences from test populations indicated: (1) that Acer- and Betula-associated N. bebbianae represent separate sibling species whose causal origins have been lost to history, and whose incomplete sexual isolation is fortified by host-associated ecological and “physiological” isolation; and (2) that incipiently speciating Acer- and Salix-associated populations are more closely related to each other than are the two Acer-associated populations, which is consistent with the HRSH. This study thus illustrates the consequences of host-related selection for both the origin and maintenance of reproductive isolation. More important, it provides evidence that the pleiotropic effects of natural selection promote allopatric speciation.     

THE GENETIC STRUCTURE OF HOST PLANT ADAPTATION IN A SPATIAL PATCHWORK: DEMOGRAPHIC VARIABILITY AMONG RECIPROCALLY TRANSPLANTED PEA APHID CLONES

Populations of insect herbivores that feed on several host plant species may experience different selective forces on each host. When the hosts cooccur in a local area, herbivore populations can provide useful models for the study of evolutionary mechanisms in patchy environments. A first step in such a study involves determination of the genetic structure of host adaptation in the region: how is genetic variation for host use structured within and between subpopulations of herbivores on each host? The structure of genetic variation for host use reveals patterns of local adaptation, probable selective consequences of migration between hosts, and the potential for further evolution. To estimate the population structure of host adaptation in a patchwork, 7–11 pea aphid clones were collected at the beginning of the summer from each of two alfalfa and two red clover fields within a very localized area (about 15–20 km²). Using a reciprocal transplant in the field, replicates of these 35 clones were allowed to develop individually on each of the two crops. A complete life table was made for each replicate. Individual fitness was calculated from the life tables as the expected rate of population increase; longevity, age at first reproduction, and total fecundity were also measured for each clonal replicate. Currently, experimental estimates of genetic variation in complete life tables are virtually nonexistent for natural populations, even for single environments (Charlesworth, 1987); field studies are even less common. Because clones from each of two source crops were tested reciprocally on both hosts, variation in relative genotypic fitness on alfalfa and clover could be partitioned among clones within source crops, between fields of the same crop, and between source crops (alfalfa or red clover), providing a view of population structure. Significant clonal variation in relative performance on alfalfa and red clover was found: clones tended to have higher fitness on the crop from which they had been collected (the “home” crop) than they did on the “away” crop, suggesting local adaptation in response to patchy patterns of selection. Clonal variability within collections from the two crops suggests the potential for changes in the genetic constitution of these aphid populations within established fields as a result of clonal selection during the summer season. Significantly negative genetic correlations across crops were found for fitness and its major components. The possibility that these negative cross-environment correlations could act as evolutionary constraints on adaptation to the patchwork is considered.     

A COMPARISON OF HIGH AND LOW VOLUME SPRAYS FOR CONTROL OF THE BEAN APHID, APHIS FABAE SCOP. ON FIELD BEANS

Insecticides were sprayed in different amounts of water to control Aphis fabae Scop. attacking spring-sown field beans. The single application of each insecticide was timed to coincide with the end of aphid migration from the winter host to the crop. A tractor-mounted row-crop hydraulic sprayer was used.
In one experiment seven different insecticide sprays were compared at high volume (in 140 gal. of water per acre); the most effective were nicotine at 22.4 oz. of active constituent per acre, demeton at 5.6 oz. and demeton-methyl at 11.2 oz.
A further comparison was made of five insecticides for each of which a selected dose of active ingredient was applied in 60 gal. (medium volume) and in 10 gal. of water per acre (low volume). The amount of insecticide retained on the plant following the low-volume application was not less than that from the medium-volume spray; the efficiency of A. fabae control was not affected by the volume sprayed except with malathion which did better at the medium volume. The systemic insecticides demeton-methyl at 6 oz. of active constituents per acre, the related compound 4741 at 3 oz. and fluoroacetamide at 3 oz. stopped the aphid numbers from rising above a peak of eight per plant compared with 230 per plant for malathion (low volume) at 12 oz. 2400 per plant for lindane at 6 oz. and 3550 per plant for check treatments sprayed with wetter only. Grain yields ranged from around 4 cwt. per acre on check treatments to around 27 cwt. per acre on plots sprayed once with the systemic insecticides. There was a curvilinear relationship between grain yield and log number of A. fabae per plant.     

GENERAL-PURPOSE GENOTYPES FOR HOST SPECIES UTILIZATION IN A NEMATODE PARASITE OF DROSOPHILA

The nematode Howardula aoronymphium parasitizes several species of mushroom-feeding Drosophila. A survey of isofemale strains of H. aoronymphium and a 25-generation selection experiment revealed that this species does not comprise host races, and that it harbors little heritable variation for adaptation to specific hosts No tradeoffs in performance on the different host species were evident. General-purpose genotypes, which can utilize all host species, characterize H. aoronymphium. An important feature of the natural history of these nematodes—correlated epidemiology across host species—is postulated to be both a cause and a consequence of the evolution of general-purpose genotypes in this species.     

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.     

THE POTENTIAL FOR COEVOLUTION IN A HOST-PARASITOID SYSTEM. II. GENETIC VARIATION WITHIN A POPULATION OF WASPS IN THE ABILITY TO PARASITIZE AN APHID HOST

Much of the study of coevolution has focused on the adaptations that have resulted from interactions between species. For reciprocal evolution to occur, there must be genetic variation in each species for traits that directly affect their interaction. Here I report evidence of significant additive genetic variance within a population of parasitic wasps in the ability to successfully parasitize an aphid host. These data, combined with companion work documenting clonal variation in a population of aphids from the same site, provide evidence that within the same population both a host and its parasitoid have the potential for specific and reciprocal genetic interactions.     

THE GENETIC ARCHITECTURE OF A COMPLEX ECOLOGICAL TRAIT: HOST PLANT USE IN THE SPECIALIST MOTH,HELIOTHIS SUBFLEXA

We used genetic mapping to examine the genetic architecture of differences in host plant use between two species of noctuid moths, Heliothis subflexa, a specialist on Physalis spp., and its close relative, the broad generalist H. virescens. We introgressed H. subflexa chromosomes into the H. virescens background and analyzed 1462 backcross insects. The effects of H. subflexa‐origin chromosomes were small when measured as the percent variation explained in backcross populations (0.2–5%), but were larger when considered in relation to the interspecific difference explained (1.5–165%). Most significant chromosomes had effects on more than one trait, and their effects varied between years, sexes, and genetic backgrounds. Different chromosomes could produce similar phenotypes, suggesting that the same trait might be controlled by different chromosomes in different backcross populations. It appears that many loci of small effect contribute to the use of Physalis by H. subflexa. We hypothesize that behavioral changes may have paved the way for physiological adaptation to Physalis by the generalist ancestor of H. subflexa and H. virescens.     

THE RESPONSE TO SELECTION FOR FAST LARVAL DEVELOPMENT IN DROSOPHILA MELANOGASTER AND ITS EFFECT ON ADULT WEIGHT: AN EXAMPLE OF A FITNESS TRADE-OFF

A selection experiment using Drosophila melanogaster revealed a strong trade-off between adult weight and larval development time (LDT), supporting the view that antagonistic pleiotropy for these two fitness traits determines mean adult size. Two experimental lines of flies were selected for a shorter LDT (measured from egg laying to pupation). After 15 generations LDT was reduced by an average of 7.9%. The response appeared to be controlled primarily by autosomal loci. A correlated response to the selection was a reduction in adult dry weight: individuals from the selected populations were on average 15.1% lighter than the controls. The lighter females of the selected lines showed a 35% drop in fecundity, but no change in longevity. Thus, there is no direct relationship between LDT and adult longevity. The genetic correlation between weight and LDT, as measured from their joint response to selection, was 0.86. Although there was weak evidence for dominance in LDT, there was none for weight, making it unlikely that selection acting on this antagonistic pleiotropy could lead to a stable polymorphism. In all lines, sex differences in weight violated expectations based on intrasex genetic correlations: Females, being larger than males, ought to require a longer LDT, whereas there was a slight trend in the opposite direction. Because the sexual dimorphism in size was not significantly altered by selection, it appears that the controlling loci are either invariant or have very limited pleiotropic effect on developmental time. It is suggested that they probably control some intrinsic, energy-intensive developmental process in males.     

ECOLOGICAL HISTORY AND EVOLUTION IN A NOVEL ENVIRONMENT: HABITAT HETEROGENEITY AND INSECT ADAPTATION TO A NEW HOST PLANT

Environmental heterogeneity has often been implicated in the maintenance of genetic variation. However, previous research has not considered how environmental heterogeneity might affect the rate of adaptation to a novel environment. In this study, I used an insect-plant system to test the hypothesis that heterogeneous environments maintain more genetic variation in fitness components in a novel environment than do uniform environments. To manipulate recent ecological history, replicate populations of the dipteran leafminer Liriomyza trifolii were maintained for 20 generations in one of three treatments: a heterogeneous environment that contained five species of host plant, and two uniform environments that contained either a susceptible chrysanthemum or tomato. The hypothesis that greater genetic variance for survivorship and developmental time on a new host plant (a leafminer-resistant chrysanthemum) would be maintained in the heterogeneous treatment relative to the uniform environments was then tested with a sib-analysis and a natural selection experiment. Populations from the heterogeneous host plant treatment had no greater genetic variance in either larval survivorship or developmental time on the new host than did populations from either of the other treatments. Moreover, the rate of adaptation to the new host did not differ between the ecological history treatments, although the populations from the uniform chrysanthemum treatment had higher mean survivorship throughout the selection experiment. The estimates of the heritability of larval survivorship from the sib-analysis and selection experiment were quite similar. These results imply that ecologically realistic levels of environmental heterogeneity will not necessarily maintain more genetic variance than uniform environments when traits expressed in a particular novel environment are considered.