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Ecological history and evolution in a novel environment: habitat heterogeneity and insect adaptation to a new host plant.

The evolution of a trait exposed to novel selective forces depends both on the intensity of selection imposed on the trait and on its additive genetic variance in the new environment (Lande 1976; Futuyma 1986; Falconer 1989; Hartl and Clark 1989). The recent ecological history of a population can influence both of these components of evolution and may thereby alter the rate or outcome of evolutionary change in a new environment. In particular, the degree of environmental heterogeneity and the similarity of current to future environments are two aspects of the ecological history of a population that may influence the process of adaptation when a population encounters a new environment.

The extent to which environmental heterogeneity (different numbers and kinds of environments) affects patterns of genetic variances has been actively studied by both theoretical and experimental population geneticists. Although the conditions are often quite restrictive, several one- and two-locus population genetic models (reviewed by Hedrick et al. 1976; Hedrick 1986) and a quantitative genetic model (Gillespie and Turelli 1989) have found conditions in which more genetic variation in fitness can be maintained in heterogeneous environments than in uniform environments. Moreover, quantitative genetic models of phenotypic evolution have shown that directional or stabilizing selection, as might occur in a uniform environment, will erode genetic variance in traits under selection (Mather 1941; Bulmer 1976; Falconer 1989). However, none of these models consider the effects of natural selection in heterogeneous versus uniform environments on genetic variation expressed in novel environments. They therefore provide little guidance toward understanding the consequences of different patterns of environmental heterogeneity on future adaptation.

Several studies have experimentally addressed the relationship between environmental variation and genetic variation and a disappointing lack of consensus has emerged. Using enzyme polymorphism in Drosophila as a measure of genetic variation, McDonald and Ayala (1974), Powell (1971), and Powell and Wistrand (1978) found that increasing environmental heterogeneity increased enzyme polymorphism whereas Long (1970), Minawa and Birley (1978), Haley and Birley (1983), and Yamazaki et al. (1983) did not. Similarly, Mackay (1980, 1981) found a positive relationship between environmental heterogeneity and additive genetic variance in adult abdominal and thoracic bristle number in Drosophila, but Garcia-Dorado et al. (1991) did not.

A problem shared by all of these studies is that they measured genetic variation in traits that may not be directly under selection in the environmental treatments imposed. For example, there is no obvious reason to believe that different temperature regimes will favor one enzyme phenotype over another (Minawa and Birley 1978), similarly there is no expectation that larval exposure to different concentrations of dietary ethanol would select for different numbers of adult bristles (Mackay 1980, 1981). Because the target of selection is unknown in these studies, it is difficult to conclude that natural selection has acted to alter genetic variance in the phenotypic characters of interest. These shortcomings lead Powell and Wistrand (1978) to argue that selection may have acted on traits genetically linked to the electrophoretic markers, while Mackay (1981) concluded that heterogeneous environments selected for increased heterozygosity overall. A varying degree of linkage disequilibrium between the traits actually under selection and the traits used to measure genetic variance could contribute greatly to the inconsistent results obtained in different studies.

Although electrophoretic phenotypes and bristle numbers are easily measured and they may provide good estimates of general changes in genetic variance, the dynamics of genetic markers chosen for convenience are not necessarily symmetric with those of loci that control traits under selection in a particular environment (Lande 1988; Hoffmann and Parsons 1991; Cheverud et al. 1994). For a population to track changes in its environment, there must be sufficient genetic variation in traits related to fitness in the changed environment. Thus, it is crucial that the effects of environmental heterogeneity on genetic variance in quantitative traits in a new environment be studied directly.

Another aspect of ecological history, the relative similarity of current and future environments, may also alter the dynamics of adaptation in a future environment. Natural selection in a current environment can alter the mean phenotype in a future environment if the traits expressed in the two environments are genetically correlated (Falconer 1952; Yamada 1962; Via and Lande 1985, 1987; Gomulkiewicz and Kirkpatrick 1992). Thus, the mean value of a trait such as insect survivorship expressed in a future environment (e.g., some future host plant) can be altered through correlated responses to selection in the current environment. A population that is more fit in the future environment (preadapted) due to a correlated response to selection in its current environment will have an increased probability of successful colonization and a reduced intensity of selection in the novel environment.

In this study, I manipulated the ecological history of experimental populations in an attempt to affect the genetic variance of quantitative traits. The principal question addressed by this study is whether a heterogeneous habitat containing five common host plants would maintain greater additive genetic variance in important components of fitness on a novel host plant than would be maintained in environments with just a single host species. As a secondary issue, I explored the effect of similarity between current and future host plants on both the mean of performance and the genetic variance in two fitness components on the new host plant. I manipulated the ecological history of laboratory populations of leafminers by maintaining replicate population cages with different host plant compositions and variabilities for 20 generations. After the treatments, I estimated the means and genetic variances of two fitness components (larval survivorship and egg-adult development time) for each treatment population on a novel leafminer-resistant host plant, using a sib-analysis. I then estimated the realized heritability of larval survivorship from a replicated natural selection experiment on treatment populations in cages containing only the leaf-miner resistant host plant.

MATERIALS AND METHODS

Study Organism

The leafminer, Liriomyza trifolii (Diptera: Agromyzidae), is a polyphagous herbivore recorded from more than 400 species of host plants including vegetables and chrysanthemums (Minkenberg and van Lenteren 1986; Parrella 1987). Although the species has a broad host range, it is doubtful that individual populations or genotypes have high performance on more than a few hosts. In a closely related species, Liriomyza sativae, Via (1984) found significant genotype x environment interactions among leafminers on two common host plants suggesting, that individuals were not generalized feeders. Moreover, population-level specialization in performance and behavior by L. trifolii on the locally predominant host plant has been reported for several crops (Bethke et al. 1987; Zehnder and Trumble 1984).

Liriomyza trifolii females insert eggs singly under the epidermis of the host leaf, and the eggs hatch in 2-4 days. The larvae create characteristic tunnels through the leaf tissue as they feed. Larval development is completed in 5-20 days after which the larva crawls out of the leaf tissue and pupates, usually after dropping to the ground. The entire life cycle takes 14 -45 days, depending on temperature and host plant quality (Parrella 1987).

This study concerned the effects of ecological history on the evolutionary potential of two traits related to performance on the host plant: larval survivorship (the proportion of larvae on a leaf that become pupae), and egg-adult developmental time. These traits are good measures of fitness because of their obvious demographic importance and because they are known to be sensitive to host plant cultivar, fertilizer regime, etc. (Bethke et al. 1987; DeJong and Van De Vrie 1987; Trumble and Quiros 1988; De Jong and Rademaker 1991).

It is very difficult to observe leafminer eggs without also damaging the leaf or the egg. Fortunately, very young mines are easily seen. For this reason, I have used the number of mines on a leaf as a surrogate of the number of viable eggs in that leaf. Although the number of eggs in a leaf will be underestimated if an egg dies before hatching, De Jong and Rademaker (1991) have shown that egg mortality is not an important source of variation in fitness in this species.

Construction of the Base Population

Larvae and pupae of L. trifolii were collected from many different host plants in locations across southern Florida. The base population was founded by 2129 flies (890 from tomato, 349 from celery, 218 from bean, 412 from lettuce, 7 from pepper, 57 from eggplant, 84 from boc-choi, 79 from u-choi, 1 from Chinese cabbage, and 32 from nightshade) [ILLUSTRATION FOR FIGURE 1 OMITTED]. It was maintained on tomato, watermelon, lettuce, lima bean, and celery in a single cage (117 x 152 x 51 cm) with a transparent plastic roof and nylon mesh walls. An elevated, metal mesh floor supported eight 100 [mm.sup.2] pots of each host. The cage was illuminated with six 40-watt fluorescent lamps on a 16L:8D photoperiod in a walk-in growth chamber maintained at 26.5 [degrees] C and 75% RH. The base population was maintained for 11 generations before the start of the experiment to allow adaptation to the laboratory environment and to reduce linkage disequilibrium that could have resulted from sampling across several leafminer populations. The population size throughout this period was an estimated [10.sup.3]-[10.sup.4] individuals.

Establishment of the Ecological History Treatments

To manipulate ecological history, three replicates of each of three types of treatment cage were initiated [ILLUSTRATION FOR FIGURE 1 OMITTED]: heterogeneous host plant cages containing five species of host plant (tomato, watermelon, bean, lettuce, and celery), and two sets of uniform host plant cages, one set containing only tomato (Lycopersicon esculentum cultivar [hereafter cv.] Sunny) and the other set containing a susceptible cultivar of chrysanthemum Chrysanthemum mortifolium cv. Manatee Iceberg). Treatment population cages were half the size of the cages that housed the base population (117 x 76 x 51 cm). The three replicate cages of each treatment were each colonized with 260-285 individual leaf miner pupae randomly sampled from the base population.

I sought to create an ecologically relevant set of experimental environments. The five plant species in the heterogeneous treatment were chosen because they are common components of the leafminer habitat in Florida and because they come from five different plant families (Solanaceae, Cucurbitaceae, Leguminosae, Umbelliferae, and Compositae). Tomato and chrysanthemum were selected as the uniform host plant treatments because they are common host plants of this leafminer. Preliminary experiments revealed that the base population, collected almost entirely from vegetables, had higher larval survivorship on tomato (96%) than on the susceptible chrysanthemum cultivar (73%), and egg-adult developmental time was 2.3 d slower (14%) on the susceptible chrysanthemum than on tomato (Hawthorne 1993).

The novel host plant, was a leafminer resistant chrysanthemum (cv. Mountain Peak). When compared to tomato and the susceptible mum, the novel host reduced the mean larval survivorship of the base population by 50% and 25% and increased mean developmental time by 5.5 and 3 d, respectively (Hawthorne 1993).

Regarding these treatments and genetic variance in performance on the new host, I hypothesized that the heterogeneous host plant treatment would maintain the most genetic variation in traits related to host plant use, that the relatively benign uniform tomato environment would contain an intermediate amount of genetic variance, and that the populations in the uniform chrysanthemum treatment would contain the least as a result of directional selection for increased performance on that plant.

Plant Culture. - All plants were grown in a temperature controlled (22 [degrees] [+ or -] 4 [degrees] C) greenhouse under supplemental lighting (16L:8D). The tomato, lettuce (cv. Black Seeded Simpson), watermelon (Sugar Baby), lima bean (Henderson Bush), and celery (June Belle) were grown from seed. The chrysanthemums, hereafter mums, were transplanted as rooted cuttings. Plants were grown in 100 [mm.sup.2] pots in potting medium, and fertilized with 15-16-17 soluble fertilizer. The vegetables used in the treatment cages were three-five weeks old, except celery which was 10-20 wk old. Mums were used in the experiments four weeks posttransplant.

Sib-Analysis on the Novel Host Plant

After 20 generations in the ecological history treatments, the additive genetic variance in larval survivorship and developmental time on the novel host was estimated. Randomly selected males from each cage (sires) were each mated to five females (dams) from the same cage and the survivorship and developmental time of their offspring on the resistant mum was measured. Twelve half-sib families were formed from each replicate cage (three families in each of four time blocks) creating up to 36 half-sib families tested per treatment, although only 33 families were actually evaluated from the tomato treatment and 35 from the heterogeneous treatment. Following mating, each dam was placed individually for oviposition into an organdy bag that enclosed a single leaf of the resistant mum (standardized for age and position). Dams were caged on separate plants for 24 h, after which they were transferred to a second enclosed leaf on a new plant (still the resistant mum) and were again allowed to oviposit for 24 h. After oviposition, all plants were randomized with respect to position in the greenhouse and plant position was changed daily to minimize systematic microenvironmental variation. First instar larvae in each leaf were counted five days following oviposition, and pupae were collected from the organdy bags 15 days following oviposition and placed into petri dishes with tight fitting lids. Each pupa was checked daily for eclosion to determine the mean development time of larvae in each leaf. Each leaf constitutes an independent observation of developmental time and larval survivorship. The percentage of larvae that survived on individual leaves was probit transformed for analysis as a threshold character.

Univariate analysis of variance (ANOVA) was performed on the sib-analysis data to determine whether treatment populations differed in larval survivorship or developmental time on the resistant mum. Treatment was a fixed effect, time-block, sire (nested within block x treatment), dam (nested within sire), and the treatment x block interaction were random effects. F-statistics were calculated with main effect mean squares tested over the appropriate interactions term(s) (PROC GLM, SAS Institute 1989).

An ANOVA was also done within each treatment to test for significant additive genetic variance by testing for significant differences among sires. Within each treatment, variance components were estimated for each main effect in the experiment. To improve the precision of those estimates, the half-sib families from the three replicate cages of each treatment were pooled. Variance components were calculated using restricted maximum likelihood (REML) methods (PROC MIXED, SAS Institute 1992). This procedure provides estimates of the variance components from unbalanced data, and their standard errors. The observed sire component [Mathematical Expression Omitted] was used to calculate the additive genetic variance ([V.sub.A]) of larval survivorship and developmental time for each treatment as [Mathematical Expression Omitted]. Standard errors for [V.sub.A] were calculated from the standard errors of the variance components, (SE [V.sub.A] = 4[SE [Mathematical Expression Omitted]]) and the standard error of the narrow sense heritability was calculated using Dickinson's approximation (SE [h.sup.2] = 4[SE [Mathematical Expression Omitted]]/[V.sub.p]) as described in Becker (1984). Because the total phenotypic variance ([V.sub.p]) of a probit transformed proportion is one, the narrow sense heritability ([h.sup.2]) of such a trait, in this case larval survivorship, equals its additive genetic variance ([V.sub.A]) (Wright 1934; Robertson and Lerner 1949).

Because [V.sub.A] and [V.sub.P] may depend in part on the phenotypic mean of a trait, I calculated the coefficient of additive genetic variation [Mathematical Expression Omitted] for developmental time which standardized the genetic variance in the trait for each population by the trait mean [Mathematical Expression Omitted] instead of the phenotypic variance ([V.sub.P]) (Houle 1992). I calculated a C[V.sub.A] for developmental time but not for larval survivorship because probit transformation had already removed the statistical dependence of the variance on the mean in that trait.

Selection Experiment on Novel Host Plant

I evaluated the consequences of the different ecological histories by observing adaptation of the nine treatment populations to the resistant mum. After 25 generations in the ecological history treatments, nine new population cages containing only the resistant cultivar of chrysanthemum Mountain Peak were each inoculated with 500 pupae from one of the treatment population cages (randomly sampled from all plants), thus maintaining the replicate lines from each treatment [ILLUSTRATION FOR FIGURE 1 OMITTED]. Except for the host plant, these population cages were identical in all respects to those used in the three ecological history treatments. Caged populations of leaf miners were provided with a constant supply of fresh plant material by systematically removing old plants and adding new plants (grown as described above). Each potted plant remained in the cage for 12 days. The oldest plants were replaced every four days. An unselected control cage, one of the treatment populations in the heterogeneous environment, was maintained as described above.

Measuring Performance on the Novel Host Plant. - Because of time constraints, only three of the nine selection cages could be screened for performance on the resistant mum each week. However, the generation time of these populations on the resistant mum is approximately three weeks. Thus, by initiating three selection cages (one from each treatment) weekly for three weeks and then performing one screen each week, cages were screened each generation for 10 generations (with the exceptions of the first replicate of generation one, all replicates of generation four, and the second replicate of generation nine). In each weekly screen, one replicate selection line from each treatment and the unselected control line were evaluated. Note that although I refer to the treatments as "mum," "tomato," or "heterogeneous," during the selection experiment lines derived from all treatments were maintained and tested on the resistant mum only. The labels "mum," "tomato," or "heterogeneous" used here refer to the ecological history treatments that the populations experienced before the start of the selection experiment.

To sample the offspring of the current generation, four plants of the resistant mum were introduced into each cage. The plants were trimmed before placing them in the cages so that each had six (in generations 0-5) or seven (in generations 6-10) leaves. Plants were removed from the cages after 24 h and randomly positioned in a leafminer-free growth chamber (26.5 [degrees] C, 75% RH). First, instar mines were counted on each leaf of all plants five days following their removal from the selection cages and an organdy bag was then secured around each leaf. Fifteen days after oviposition, pupae were collected from the floor of the organdy bags, counted, and placed into petri dishes with tight fitting lids. The day of eclosion of each fly was recorded so that the mean developmental time of the individuals within each leaf could be calculated. The mean larval survivorship (number of pupae/number of mines) and egg-adult developmental time for each selection line was determined each generation as the mean over all leaves and plants.

Analysis. - The mean larval survivorship and developmental time of each selection line in each generation was used to test for a response to selection. To correct for environmental trends, trait means for each replicate were subtracted from those of the unselected control line. All analyses are based on corrected values. The rate of response to selection in larval survivorship and developmental time for each replicate was estimated with linear regression. ANOVA on the replicate slopes was used to determine whether the treatments differed in their rate of adaptation to the resistant mum (Hill 1972, 1980).

Estimation of Selection Differentials and Realized Heritability. - By considering larval survivorship a threshold trait, I estimated the selection differential each generation and calculated realized heritabilities for each replicate. I then used the replicated estimates of the responses to selection and realized heritabilities to test for significant differences among treatments.

Realized heritability is a measure of the genetic variance actually available for the response to selection. Realized heritability was estimated for each selection line from the regression of the cumulative phenotypic response to selection on the cumulative selection differential (Hill 1972, 1980; Falconer 1989). These regressions were performed on probit transformed survivorships.

The selection differential of larval survivorship was estimated from the proportion of the population that survived using standard methods for threshold traits (Crow and Kimura 1970; Falconer 1989). The mean selection differential for larval survivorship in each selection line was calculated for every generation. The mean selection differential for a given replicate generation was the mean of the four plants tested in the screen. The selection differentials in generations when no screens were performed were estimated as the mean of the selection differentials in generations immediately before and after the missed generation.

To test for differences in realized heritability among treatments, ANOVA was performed on the replicate realized heritabilities of larval survivorship (Hill 1972). The significance of the mean realized [h.sup.2] of each treatment was evaluated with t-tests on the within-treatments replicates.

RESULTS

The Effect of Ecological History on Means and Genetic Variances: Sib-Analysis

Leafminer populations maintained in the uniform mum treatment had much higher initial larval survivorship in the novel environment than did populations from the other treatments ([ILLUSTRATION FOR FIGURE 2 OMITTED]; [F.sub.2,6] = 41.36, P = 0.003). However, the mean developmental time did not differ among treatment groups ([ILLUSTRATION FOR FIGURE 2 OMITTED]; [F.sub.2,6] = 3.22, P = 0.11).

There was significant genetic variance for both larval survivorship and developmental time on the new host in the uniform mum treatment populations (the sire effect in the sib analysis [Table 1]). The sire effect on developmental time in the heterogeneous treatment was marginally significant (P = 0.055) but there were no other significant sire effects for either trait in the uniform tomato or the heterogeneous host [TABULAR DATA FOR TABLE 1 OMITTED] plant treatments (Table 1). In all treatments there was a significant effect of dam for larval survivorship in the novel environment, but not for developmental time (Table 1). Maximum-likelihood estimates of the dam components of variance for larval survivorship were larger than the sire components (Table 2), indicating the presence of maternal cytoplasmic or environmental factors, and/or dominance or epistatic genetic variance (Falconer 1989). The cage effect (which may indicate that a founder event or genetic drift has acted to produce differences among the replicate cages) was significant (P = 0.037) for larval survivorship in the tomato treatment, but it was not significant for developmental time in that treatment or for either trait in the other treatments (Table 1).

Maximum-likelihood estimates of additive genetic variance ([V.sub.A]) revealed that additive genetic variance in survivorship and developmental time in the new environment was nominally, but not significantly, larger for the populations from the uniform mum treatment than for populations from the other two treatments (Table 3). Because the standard errors of [V.sub.A] are relatively large and overlap (the differences among the treatments do not exceed [+ or -] 2 SE), I cannot conclude that the estimates of genetic variance differ among treatments for either trait (cf. Mackay, 1981). The results [TABULAR DATA FOR TABLE 2 OMITTED] were similar for developmental time. The coefficient of additive genetic variation calculated for developmental time was much higher for the uniform mum treatment populations (C[V.sub.A] = 3.34) than for the populations from the heterogeneous plant (C[V.sub.A] = 0.56) or the uniform tomato (C[V.sub.A] = 0.00) treatments.

Effects of Ecological History on Genetic Variances: Natural Selection Experiment

Populations from all three ecological history treatments evolved increased larval survivorship during the selection experiment [ILLUSTRATION FOR FIGURE 3A OMITTED]. The regression coefficient of larval survivorship on generations was significant (P [less than] 0.01) for each replicate when analyzed separately (analyses not shown) and the means of the three slopes from each treatment were also significantly greater than zero [ILLUSTRATION FOR FIGURE 3A OMITTED]. However, populations from the three treatments did not differ from each other in the rate of change in larval survivorship to the resistant mum ([F.sub.2,6] = 1.31, P = 0.34).

The intercepts of the response to selection of larval survivorship in the mixed plant (-0.02) and uniform tomato (-0.06) treatments were not significantly different from zero (P = 0.55, df = 2; P = 0.47, df = 2 respectively) suggesting that neither of those treatments differed from the control before the selection experiment began. The intercept of the uniform mum treatment (0.15) was significantly greater than zero (P = 0.018, df = 2) and also significantly greater than the other two treatments (P = 0.01, df = 2). This reinforces the observation from the sib-analysis that populations that experienced natural selection on the susceptible mum had significantly increased mean larval survivorship on the resistant mum. As a consequence, populations from the uniform mum treatment had higher larval survivorship throughout the selection experiment than did populations from the uniform tomato and mixed plant treatments [ILLUSTRATION FOR FIGURE 4 OMITTED].

In contrast to the preselection estimates of VA from the sib-analysis, which suggested that there was no significant additive genetic variance in populations from two of the treatments, significant adaptation of populations from all three treatments to the resistant mum indicated that all three had significant additive genetic variance in larval survivorship (Table 3). The significant realized heritability estimates were in close agreement with the (mostly) nonsignificant estimates of narrow sense heritability from the sib-analysis (Table 3). The realized heritabilities of larval survivorship for populations in the three treatments were not significantly different from each other ([F.sub.2,6] = 3.54, P = 0.097) although they were all significantly greater than zero.

In species such as L. trifolii, with overlapping generations, a more rapid preadult developmental time usually contributes to increased fitness (Lewontin 1965; Charlesworth 1980). A decrease in developmental time during the selection experiment is therefore consistent with increased adaptation to the resistant mum. Mean developmental time decreased an average of 0.10, 0.13, and 0.15 d per generation in the heterogeneous plant, uniform tomato, and uniform mum treatments respectively over the course of the selection experiment [ILLUSTRATION FOR FIGURE 3B OMITTED] but the rate of change in developmental time did not differ among treatments ([F.sub.2,6] = 3.84, P = 0.12).
TABLE 3. Mean heritabilities ([h.sup.2]) for larval survivorship
on the resistant mum of populations with three different ecological
histories. Significance of the sib-analysis [h.sup.2] is based on
the sire main effect in the within treatment ANOVA (Table 1).
Significance of realized [h.sup.2] was evaluated by a t-test within
treatments with n - 1 = 2 degrees of freedom.

Treatment             Sib-analysis [h.sup.2]   Realized [h.sup.2]

Uniform mum                  0.293(*)               0.223(**)
Uniform tomato               0.188                  0.188(**)
Heterogeneous plant          0.124                  0.170(*)

* P = 0.015; ** P [less than] 0.005.


DISCUSSION

The 20 generations in the ecological history treatments affected the mean performance, but not the genetic variances in performance, on the novel host plant. Populations from the historically heterogeneous host plant environment did not have more genetic variation in critical components of fitness (larval viability and developmental time) in the novel environment than did populations from historically uniform environments. Although environmental heterogeneity did not influence either the mean performance, the additive genetic variance, or the realized heritability in the novel environment, the similarity of the past environment to a novel environment strongly influenced the mean performance of leafminer populations in the novel environment.

Previous experiments in heterogeneous environments (e.g., Powell and Wistrand 1978; Mackay 1980, 1981) led us to hypothesize that the populations from heterogeneous environments would maintain more genetic variation than those from the two uniform environments. Because the environmental heterogeneity in this experiment was in the form of multiple host plants I expected this excess genetic variation to be in traits related to host plant use, and I expected a more rapid response to selection on the novel host plant in the populations from the heterogeneous treatment. The experiments reported here suggest that environmental heterogeneity per se may not enhance genetic variation involved in tracking a particular changing environment. This is because there is no necessary connection between the alleles maintained in an arbitrary heterogeneous environment and those that influence fitness in a particular new environment.

The significant responses to selection seen in all treatments indicated that genetic variation in larval survivorship on the resistant mum existed in the base population and in each of the replicate populations. This variation was therefore available to be altered by the ecological history manipulations. If heterogeneous environments maintained increased genetic variance (1) by increasing genome-wide heterozygosity per se (Mackay 1981; Gillespie and Turelli 1989); (2) through the action of genotype X environment interaction (Bell 1992); or (3) by maintaining polymorphisms at particular loci (Hedrick et al. 1976; Hedrick 1986), I should reasonably have expected to observe increased genetic variance in the heterogeneous environment in this study. Given that 20 generations in the treatments was sufficient to observe changes in genetic variance in these populations of leafminers, this heterogeneous environment simply lacked the characteristics necessary to promote variation that was relevant to this particular new environment.

The results of this study imply that populations from heterogeneous environments will not (on average) adapt to unpredictable environmental change more rapidly than populations from uniform environments. Although particular combinations of environments may augment genetic variance due to significant genotype x environment interactions (Via and Lande 1985, 1987; Bell 1992), the contribution of that extra genetic variance towards a response to selection in a new environment depends on the cross-environment genetic correlations between the current and the new environments (Dickerson 1955; Via and Lande 1985, 1987; Bell 1992).

Correlated Responses to Selection: Preadaptation to the Resistant Mum. - Populations maintained in the uniform mum treatment increased their larval survivorship on the susceptible chrysanthemum during the 20 generations in that treatment (Hawthorne 1993). As a consequence of a positive cross-environment genetic correlation between survivorship on the susceptible and resistant mum cultivars (correlation of family means of larval survivorship on susceptible versus resistant mums = 0.22; Hawthorne 1993), those populations also had higher mean larval survivorship on the resistant mum than populations from the other treatments (41% vs. 20%, [ILLUSTRATION FOR FIGURE 2 OMITTED]). Because the heterogeneous plant and uniform tomato treatments had no discernible effect on the initial mean performance of the leafminers on the resistant mum it can be tentatively concluded that larval survivorship on those plants is genetically uncorrelated with larval survivorship on the resistant mum.

Estimates of Genetic Variance: Sib-Analysis versus Selection Experiment. - The estimates of genetic variance in larval survivorship on the resistant mum made in the sib-analysis were not significantly greater than zero for two of the treatments (heterogeneous and tomato). However, all three of the treatments showed significant responses to selection and the significant realized heritabilities obtained for all treatments were close to the values estimated in the sib-analyses (Table 3). Mitchell-Olds and Bergelson (1990) discuss the low probability of obtaining statistically significant genetic variances using typical sample sizes in a sib-analysis, especially when the real genetic variance is small, as in this study. The problem lies in distinguishing between the absence of genetic variance and accurate but nonsignificant estimates resulting from a limited sample size. These results clearly illustrate the danger in concluding that a nonsignificant, but positive, estimate of genetic variance or heritability indicates a lack of genetic variance.

Implications for Conservation Biology and Biological Control. - Preadaptation such as that observed in the uniform mum treatment populations could have important practical consequences. Although all replicates of each treatment avoided extinction when restricted to the resistant mum, the probability of extinction of nonpreadapted populations might have been much higher on a slightly more hostile plant. The experimental scenario devised in this study has obvious implications for conservation biology and biological control in which organisms are collected in one environment and released in another possibly different environment.

The experiments reported here indicate that environmental heterogeneity is not a reliable indicator of the genetic diversity in ecologically important traits when they are expressed in novel environments. Therefore, populations from historically heterogeneous populations may not adapt more readily to novel environments than do populations from uniform environments. These results suggest that special efforts to collect samples of exotic biological control agents or endangered species from a variety of different habitat types will not necessarily increase the ability of the population of interest to adapt to a new habitat following introduction. Moreover, efforts to maintain genetic variation in captive populations of endangered species through maintenance in heterogeneous environments (Hoffman and Parsons 1991) may not be more effective in allowing those populations to evolve in a novel environment than simple maintenance in a uniform environment. However, the results described here do suggest, that given a number of potential sources for the introduced individuals, source(s) from habitat(s) most similar to the new habitat should be used. Extra resources could then be applied toward increasing the sample size within the chosen habitats and maintaining a larger effective population size.

Adaptation to local environments can often occur quite rapidly. The genetic changes that occur during adaptation to the current environment may influence the ability of a population to adapt to future environmental change, and may therefore influence the probability of local extinction in the future environment. The measurement of genetic variances and selection intensities in a novel environment allows the prediction of evolutionary trajectories for particular traits in a population introduced into that environment. The measurement of genetic covariances in ecologically important traits (e.g., survivorship) between the current and future environments and the intensity of selection in the current environment may provide additional useful information on the future consequences of adaptation of populations to a current environment.

ACKNOWLEDGMENTS

I thank Sara Via for providing research facilities and guidance and Yoder Brothers, Inc., for the chrysanthemums. I thank W. Tingey, R. Harrison, T. Dennehy, C. McCulloch, D. Winkler, J. Conner, F. Hyland, H. Henter, K. Hural, and T. Dorsey for their help. D. Schuster, S. Webb, K. Schuler, and K. Pohroneseny helped greatly with the leafminer collections. A. Kaveh and E. Schott admirably counted mines and reared plants. This research was partially funded by a National Science Foundation Dissertation Improvement Award (BSR-9100851), by Sigma Xi, and by the Andrew Mellon Foundation.

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