Experimental evolution in ChlamydomonasII. Genetic...

*Correspondence. E-mail: [email protected]†Present address: Laboratoire de Malherbologie, INRA, B.V.1540, 21034 Dijon Cedex, France.

Heredity 78 (1997) 498–506 Received 10 June 1996

Experimental evolution in Chlamydomonas II.Genetic variation in strongly contrasted

environments

GRAHAM BELL* & XAVIER REBOUD†Redpath Museum and Department of Biology, McGill University, 859 Sherbrooke Street West, Montreal, Quebec,

Canada H3A 2K6

Experimental populations of Chlamydomonas were selected in Light (photoautotrophic) orDark (heterotrophic) environments. Each population was a clone, founded by a single sporeand propagated vegetatively thereafter. A heterogeneous environment was simulated by mixingLight and Dark lines in each growth cycle and redistributing them between the two environ-ments in the next cycle. Some lines maintained permanently in the Dark evolved greatlyincreased growth within fewer than 300 generations, at the expense of reduced growth in theLight. Lines maintained in both Light and Dark environments evolved a negative geneticcorrelation between Light and Dark growth, and displayed more genetic variance of fitnessthan lines maintained in either environment exclusively. It is possible that genetic variancenear mutation–selection balance is greater in heterogeneous environments because selection isweaker. However, the evolution of distinctly specialized lineages in these experiments suggeststhat in the conditions of batch culture a cost of adaptation creates negative frequency-depend-ent selection that maintains genetic variance. Genetic variance was greater in the morepermissive environment (Light) than in the more restrictive environment (Dark).

Keywords: autotroph vs. heterotroph, Chlamydomonas, correlated response, cost of adapta-tion, fitness, genetic variance, selection experiment.

Introduction

It is widely accepted that environmental hetero-geneity may support genetic diversity, either tran-siently through obstructing selection and retardingthe loss of genetic variance, or permanently throughthe maintenance of a stable genetic equilibriumunder disruptive selection (Levene, 1953; MaynardSmith & Hoekstra, 1980; Via & Lande, 1985;Hedrick, 1986). In a previous paper, using theunicellular chlorophyte Chlamydomonas as a modelsystem, Bell (1997) has shown how selection in adiverse environment, consisting of a range of culturemedia with different concentrations of macronutri-ents, was associated with higher levels of geneticvariance in fitness than selection in a comparableuniform environment. This result is consistent withsurveys of genotypic variance, which have shown thatthe genetic correlation between environments differ-

ing in the dilution of macronutrients declinedtowards zero as environmental variance increased,but did not become consistently negative (Bell,1992). It might be argued that the effect will bemuch greater when environments differ qualitatively,rather than merely quantitatively. We might thenanticipate that genetic correlations will becomenegative through antagonistic adaptations todifferent environments — a general ‘cost of adapta-tion’ — and that in consequence populations thatexperience both, or all, environments will be muchmore variable than those that experience only one.More specifically, we can define six propositionsdescribing how genetic variance in fitness is expectedto be maintained in populations that are exposedsimultaneously to qualitatively differentenvironments.

1 Allopatric lines (maintained in isolation) willbecome adapted to a novel or stressfulenvironment.

2 Adaptation will be specific: the direct response toselection will be greater than any indirect

©1997 The Genetical Society of Great Britain.498

SELECTION IN HETEROGENEOUS ENVIRONMENTS 499

response in other environments, creating a nega-tive genetic correlation across environments.

3 This negative correlation is caused in part by acost of adaptation, advance over the foundinggenotype in the environment of selection beingassociated with regress in other environments.

4 Sympatric populations that are regularly distrib-uted among environments will show less specificadaptation to a given environment than allopatricpopulations that are maintained in that environ-ment only, but they will also show less regress inother environments.

5 Selection in sympatric lines that experience avariety of conditions of growth is less effectivebecause genes that improve performance in oneenvironment but reduce it in others will be fixedmore slowly, if at all; this will create a negativegenetic correlation within sympatric populations.

6 Consequently, the genetic variance of fitness willbe greater in sympatric than in allopatrictreatments.

This paper is an attempt to investigate thesepropositions in an experimental system using Chla-mydomonas, and thus to evaluate the argumentlinking environmental heterogeneity to geneticdiversity. Our experimental populations are clonesthat are propagated vegetatively; consequently, thegenetic variances and covariances that we estimateare the consequence of novel mutations that havearisen during the course of the experiment. Ourresults are not therefore influenced by any pre-exist-ing genetic variances or covariances in the basepopulations.

Materials and methods

Base populations

The base population for each selection line was asingle spore. Two mt+ (CC-1010 and CC-2343) andtwo mtµ (CC-1952 and CC-2342) strains of Chlamy-domonas reinhardtii were crossed in all combina-tions, and from each cross one mt+ and one mtµ

spore were isolated, a total of eight selection lines.Routine laboratory procedures are described byHarris (1989).

Environmental treatments

The two physical environments used were:

d Bold’s minimal liquid medium, under continuousillumination (Light treatment);

d the same medium supplemented with 1.2 g Lµ1

sodium acetate, kept dark (Dark treatment).

In both cases, the cultures comprised 300 mL ofmedium in 500 mL Erlenmeyer flasks bubbled withsterile air; Light and Dark flasks were maintained onthe same shelf, the Dark flasks being wrapped inaluminium foil. The over-riding difference betweenthe two environments was thus the wholly photo-autotrophic growth in one and wholly heterotrophicgrowth in the other.

Environmental heterogeneity was created bymixing Light and Dark cultures. In the allopatrictreatment, Light and Dark cultures were maintainedseparately. In the sympatric treatment, Light andDark cultures were mixed after each cycle of growth,the mixture being used to inoculate both Light andDark flasks at the beginning of the next cycle. Theallopatric treatment thus represents a uniformenvironment, and the sympatric treatment a diverseor heterogeneous environment.

Each of the eight founding spores gave rise tothree selection lines: an allopatric line maintained inthe Light, an allopatric line maintained in the Dark,and a sympatric line. These were unreplicated.There were thus 24 selection lines in all.

Selection

The experiment was propagated by serial transfer ofasexual cultures for one year, at the end of whichthe Light lines had completed 66 cycles of growthand the Dark lines 24 cycles. Each transfer involvedinoculating 100 mL of culture (26Å104 cells) into300 mL medium, permitting 11–12 doublings (to afinal population size of roughly 2Å108 cells) percycle; Light lines thus completed about 750 genera-tions and Dark lines about 275 generations.

Assay

After selection, spores were isolated from each lineand from its founder, the eight founding genotypeshaving been stored meanwhile on solid medium indim light. Four spores were isolated from each flask;the sympatric lines were thus each represented byeight spores, four from the Dark flask and four fromthe Light flask of the final cycle. Each spore wasthen grown in Dark and Light conditions, exceptthat the assay was carried out (for reasons of practi-cality) in culture tubes rather than in flasks. Singlecolonies from plates were grown in 10 mL of liquidmedium in culture tubes for 5 days, at which pointthey were in vigorous growth. These preinoculation

© The Genetical Society of Great Britain, Heredity, 78, 498–506.

500 G. BELL & X. REBOUD

cultures were then diluted to a standard opticaldensity, and used to inoculate 20 mL of freshmedium with 100 mL of culture. Two replicatecultures of each genotype–environment combinationwere used. Growth was measured on a spectropho-tometer at intervals of about two days, providingcomplete growth curves from which the logisticparameters r and K can be estimated, althoughgrowth was markedly nonlogistic in some Darkcultures. The measure of growth analysed here is theoptical density of the culture after 10 days, P10. Thisis a simple and model-free statistic that reflects bothr and K, and is closer to fitness in the circumstancesof the experiment than either. The results reportedhere, particularly the response to selection in allo-patry and the greater genetic variance of the sympat-ric lines, apply quantitatively to r and K as well as toP10. The relationship between r and K in the evolvedpopulations will be described in a later paper. Theassay thus comprised 5 flasks (the three experi-mental treatments, the sympatric treatment beingrepresented by two flasks, plus the founder)Å8linesÅ4 sporesÅ2 environmentsÅ2 replicates = 640cultures.

Because the conditions of growth in the selectionenvironment (flasks) and in the assay environment(tubes) were somewhat different, the assay proce-dure was itself tested, after the completion of theexperiment. Forty independent isolates of C. rein-hardtii were grown in replicated flask and tubecultures, in Light and Dark conditions, in order toestimate the genetic correlation between flask andtube growth.

Results

Assay procedure

Discrepancies between flask and tube scores mayarise from two sources: error variance (whichreduces the correlation between scores of replicatecultures in either flasks or tubes) and systematicdifferences between flask and tube environments.The correlation between flask and tube scores, inde-pendently of error, can be estimated as the intraclassgenetic correlation coefficient:

tG = s 2G /[s 2

G+s 2GE],

where G refers to genetic main effects and GE togenotype–environment interaction, the environmentbeing flask vs. tube. Estimates from the flask–tubeassay were:

Light growth: s 2G = 1887; s 2

GE = 535; tG = 0.78.

Dark growth: s 2G = 14 419; s 2

GE = 14 979; tG = 0.49.

Estimates of the genetic variance were highly signi-ficant (Ps0.001) in both cases; genotype–environ-ment interaction was significant for Dark growth(Ps0.01) but not for Light growth (Pa0.1).

Light and Dark growth

The genetic variance of growth is similar among the40 isolates scored for the flask–tube assay andamong the eight founding spores of the main experi-ment. In both cases the variance of Dark growth isabout an order of magnitude greater than the vari-ance of Light growth. All isolates are capable ofgrowing well in the light, but there is a wide range ofbehaviour in the dark, some isolates growing as wellas they do in the light, whereas others can scarcelygrow at all. The Dark environment is thus the morestressful, in the sense that the algae are initially lesswell-adapted to it.

Response to selection in allopatry

The population statistics before and after selectionare given in Table 1. The response to selection canbe evaluated in two ways. In the first place, all pairsof Light and Dark lines were tested both in theenvironment of selection and in the other environ-ment. The interaction of selection environment withassay environment (Light lines growing better thanDark lines in the Light environment but worse in theDark environment, and vice versa) shows that selec-tion has caused sister lines exposed to differentenvironments to diverge. This effect was significant(at a level per test of 0.05/8 = 0.00625) in six of eightcases. Secondly, a comparison of each line with itsfounder, tested in the environment of selection,shows whether selection has substantially increasedadaptedness to that environment. Two lines (Bµand Dµ) evolved a markedly enhanced ability (rela-tive to their founders) to grow in the Dark, butotherwise the degree of adaptation, in Light orDark, was modest. The overall increase of adapted-ness in the Dark was not formally significant,primarily because the variance among lines wasinflated by the highly exaggerated response of theBµ and Dµ lines. In both environments, thegenetic variance within lines was low at the begin-ning of the experiment, and increased markedly overtime. In the Light environment, the variance amonglines increased during the course of the experiment;in the Dark environment, the variance among linesremained the same or decreased.



Correlation of Light and Dark growth

The growth of Light and Dark allopatric lines inboth environments is shown in Fig. 1. It is clear thatthe Light and Dark lines have diverged: in seven ofthe eight lines, the Dark lines grow better in the

Dark and worse in the Light, whereas the Light linesgrow better in the Light but worse in the Dark. Thiseffect is highly significant in most cases (Table 1,SelectionÅAssay interaction). The probability thatthe direction of the divergence (lines more highlyadapted in the environment of selection, less highlyadapted in the other, in seven of eight cases)resulted from chance is 9/256 = 0.035. Selection hasthus created negative genetic correlation betweenisolated populations within a few hundredgenerations.

Cost of adaptation

The divergence of Light and Dark lines need notreflect a cost of adaptation: it is conceivable thateach line exceeds its founder in either environment,as the result of adaptation to general features oflaboratory culture. There is a cost of adaptation onlyif increased growth in the Dark is accompanied by


Table 1 Response to selection in allopatry. Scores areoptical density at 10 days. The table shows the meangrowth in environment B of spores selected inenvironment A, YAB, where L = Light, D = Dark andF = Founder. Means are based on two replicate culturesof each of four spores from each line

Line YLL YLD YDL YDD YFL YFD

A+ 658 174 544 316 585 362Aµ 673 55 484 419 609 380B+ 561 88 480 237 635 242Bµ 612 39 340 293 669 40C+ 654 149 563 462 633 446Cµ 371 466 517 416 524 400D+ 617 160 523 436 640 354Dµ 517 367 349 590 617 220Mean 583 187 475 396 614 305

Divergence caused by selection can be evaluated for eachline, because spores should grow better in theenvironment in which they were selected. Spores isolatedfrom Light and Dark selection lines were all tested inboth Light and Dark conditions, with two replicates ofeach genotype–environment combination.The model was thus:

Source df

Selection environment 1Assay environment 1SelectionÅAssay 1Spores within lines 12Replication 16

The occurrence of selection is detected by theSelectionÅAssay interaction; this was tested by theSpores mean square, unless it were smaller than theReplication MS, in which case the Replication MS wasused instead. The results of this line-by-line analysis were:

Line F P

A+ 9.6 0.021Aµ 56.1 s0.001B+ 5.6 0.056Bµ 90.0 s0.001C+ 26.5 0.002Cµ 9.9 0.005D+ 21.2 0.004Dµ 23.1 0.003

Table 1 ContinuedOverall means and variances are as follows

Variance components

Among WithinTreatment Mean SE (mean) lines lines Error

LightBefore

selection 614 14 1490 131 4655After

selection 583 33 8647 3330 5102DarkBefore

selection 305 46 16 811 1605 1988After

selection 396 36 10 469 7059 1241

The specificity of the response to selection can beevaluated by comparing lines tested in the environmentwith the founders, tested in the same environment. This ishighly significant (Ps0.001) in only two cases, Bµ andDµ selected in the Dark. The mean difference betweenlines selected in the Light and their founders was µ31(SE 28, t7 = µ1.1, Pa0.25). The mean difference betweenlines selected in the Dark and their founders was +91(SE 51, t7 = 1.8, P20.1). The error variance does notchange during the experiment. The variance within lines(genetic variance) is greater after selection (Lighttreatment, F24,24 = 25.4, Ps0.001; Dark treatment,F24,24 = 4.4, Ps0.001). The variance among lines is greaterafter selection in the Light treatment (F7,7 = 5.8,0.01sPs0.025) but did not change appreciably in theDark treatment (F7,7 = 1.6, Pa0.1).


reduced growth in the Light. Fig. 2 shows that all theDark selection lines regressed in the Light, and themost marked regress in the Light was shown by thelines that achieved the greatest advance in the Dark.

Genetic correlation in sympatric lines

The growth of spores extracted from the sympatriclines in Light and Dark environments is shown inFig. 3. There is a broad range of behaviour withinthe populations, but a tendency towards specializa-tion: spores that grow well in the Dark tend to growpoorly in the Light, and vice versa. The cost of adap-tation observed in the allopatric lines thus gives riseto a negative genetic correlation within sympatricpopulations.

Response to selection in sympatry

The growth of sympatric populations in a givenenvironment is less than that of allopatric popula-tions that have been selected in that environment(Fig. 4(a)). However, their growth in either environ-ment is greater than that of allopatric populationsthat have not been selected in that environment(Fig. 4(b)). In either case, the effect is greater in theDark than in the Light.


Fig. 1 Genetic divergence of allopatric lines. The eightselection lines obtained from the four original crosses arelabelled A+, Aµ, etc. The open circles are mean valuesfor the Light selection lines, solid circles for the Darkselection lines. Light and Dark sister lines are connectedto show the negative correlation between environments.

Fig. 2 Cost of adaptation to the Dark environment. Thevalues plotted are the deviations of the means of selectionlines from the parental spore; thus, positive values indi-cate an advance, and negative values a regress. The solidline is the least squares regression: y = µ1.11xµ63,r 2 = 0.72. This is of course strongly levered by Bµ andDµ.

Fig. 3 Light and Dark growth in sympatric lines. Eachpoint is a spore (N = 64). The genetic correlation is µ0.40(Ps0.01).


Genetic variance of fitness

Estimates of genetic variance within lines are givenin Table 2. In the Light environment, seven of eightsympatric lines yield a greater estimate than thecorresponding allopatric Light selection lines(one-tailed P = 0.035), and the means¹1 SE amonglines do not overlap. Genetic variance was onaverage nearly three times as great in sympatry as inallopatry. There was a trend in the same direction in

the Dark environment, but it was not nearly asmarked, and cannot be shown to be significant.

Discussion

Broadly speaking, these results provide experimentaldocumentation of the conventional account of howgenetic variation for site-specific fitness is main-tained in heterogeneous environments. Specificadaptation to heterotrophic conditions is accom-panied by a loss of fitness in photoautotrophicconditions, and in a heterogeneous environment thiscost of adaptation is reflected in a negative geneticcorrelation between Light and Dark growth thatretards or prevents the loss of genetic variance.

Response to selection in uniform environments

Selection was effective despite the genetic uniform-ity of the founding populations. The input of newvariation by mutation was thus adequate to fueladaptation in these large populations of 107µ108

individuals. The rate of input can be calculated fromTable 1 as:

(3330µ131)/750 = 4.265/465521Å10µ3 s 2e

per generation in the Light lines, and

(7059µ1605)/275 = 19.833/198821Å10µ2 s 2e


Fig. 4 Response to selection in allopatric and sympatriclines. Open circles indicate spores tested in the Light andsolid circles in the Dark. (a) In the upper diagram,sympatric lines are compared with allopatric lines, in theenvironment in which the allopatric lines had been selec-ted. The allopatric lines exceed the sympatric lines in13/16 cases (P = 0.021, binomial test). (b) In the lowerdiagram, sympatric lines are compared with allopatriclines, in the environment in which the allopatric lines hadnot been selected. The sympatric lines exceed the allopat-ric lines in 13/15 cases (equal values in one case)(P = 0.007, binomial test).

Table 2 Genetic variance of fitness in selection lines.Estimates were obtained by equating observed withexpected mean squares in single-classification analysis ofvariance, and may be negative. Estimates for theallopatric lines are equivalent to the ‘within lines’ variancecomponent in Table 1. The sympatric populationcompared with the allopatric Light line is that extractedfrom the Light flask of the two used to propagate thesympatric line after the last cycle of growth; similarly forthe Dark treatment

Light Dark

Line Allopatric Sympatric Allopatric Sympatric

A+ 5197 25 767 29 883 7696Aµ µ2119 12 036 7264 5831B+ µ1545 14 840 6676 13 322Bµ µ3601 µ567 9959 132C+ 2195 3429 µ359 3384Cµ 21 581 7791 1034 20 433D+ µ150 8170 1847 20 787Dµ 5080 6481 167 2776Mean 3330 9743 7059 9295SE 2849 2838 3524 2829


per generation in the Dark lines. The value of about10µ3 of the environmental variance per generation iscomparable with other guesses and estimates(Maynard Smith, 1989), although it is not clear whymicroenvironmental effects causing the variance ofreplicate cultures should provide a standard forcomparing different systems. These estimates areminimal, because some of the new variation thatappears will be harvested by selection.

The variance among the Dark lines decreasedsomewhat during the experiment because lines thatat first grew poorly became adapted to heterotrophicconditions, an example of phenotypic convergence.The divergence of the Light lines, where selectionwas ineffective, is probably spurious. It is causedsolely by the low score of the C– selection line, (aprominent outlier in Fig. 1), where three of fourspores at first grew slowly, although they laterachieved a normal asymptotic density.

Adaptive divergence and the cost of adaptation

Adaptation in experimental populations may bespecific or general: specific, in that it refers to aparticular environment among all those tested, andgeneral, in that it applies broadly to the laboratoryconditions of growth common to all treatments. Ifadaptation is to any degree specific, as in practice italmost always will be, then it will cause populationsto diverge so that the genetic correlation amongthem is negative, as in Fig. 1. This need not implythat adaptation involves a cost of adaptation, asusually understood. Adaptation is costly only ifadvance in the environments of selection is achievedat the expense of regress in other environments. Tomake this point more clearly, we have defined threenew terms in Fig. 5. These refer to selection in twoenvironments such as Light and Dark. There is adirect response, the increase of growth in theenvironment in which the population has been selec-ted, and an indirect, or correlated, response in theother environment. If both direct and indirectresponses are positive, but the direct exceeds theindirect response, selection may be said to be syncli-nal: the response to selection is in the same direc-tion in both environments. If the direct response ispositive and the indirect response zero, selection isaclinic: adaptation to one environment has no effecton growth in the other. Finally, the direct responsemay be positive and the indirect response negative:this is anticlinal selection, advance in the environ-ment of selection causing regress in the otherenvironment. It is only anticlinal selection thatimplies a cost of adaptation. Thus, the cost of adap-

tation can be evaluated only by reference to anancestor, and not solely by the divergence of linesselected in different environments.

The main response to selection in this experimentwas the adaptation to Dark growth by lines Bµ andDµ, and to a lesser extent by D+. These responseswere anticlinal, as shown in Fig. 2 by the reducedgrowth of these lines in Light conditions, relative totheir founders. Figure 6 shows in more detail the


Fig. 5 The concepts of synclinal, aclinic and anticlinalselection. The open and solid circles represent Light andDark selection lines, respectively; F indicates the founder.


behaviour of the Bµ line. There is no discernibledirect or indirect effect of selection in the Light; inthe Dark, the line evolves greatly improved growth,but no longer grows as well in the Light. (In paren-thesis, we note that after about 150 generations thisline grew yellow in the dark. Genes causing thischaracter are well known; they arise as a lesion inthe final stage of the synthesis of chlorophyll in thedark, leading to an accumulation of protochlorophyl-lide. Whether or not this character in itself causesgreater fitness in the Dark has not beeninvestigated.)

The only directly comparable experiment invol-ving large asexual populations cultured for hundredsor thousands of generations (Bennett et al., 1992;Bennett & Lenski, 1993) showed that adaptation todifferent temperatures by allopatric lines of E. coliover 2000 generations was not always, or evenusually, accompanied by decreased performance atother temperatures, relative to the ancestral strain.There is some evidence for a cost of adaptationfrom reciprocal transplant experiments, both innatural environments (Antonovics & Primack, 1982;van Tienderen, 1992) and in environments severelydisturbed by human activity (Davies & Snaydon,1976).

Response to selection in heterogeneousenvironments

In heterogeneous environments, selection may varyin direction at different sites, or in different condi-

tions of growth. Local (within-site) regulation ofdensity, as in the original model by Levene (1953),creates negative frequency-dependent selection thatmay retain genetic variance for site-specific fitnesspermanently in the population, although the condi-tions for stable genetic equilibrium are quite severe(Maynard Smith & Hoekstra, 1980; Via & Lande,1985; Gillespie & Turelli, 1989). A less oneroushypothesis is that directional selection is less intensein heterogeneous environments, so that genetic vari-ance, although eventually eliminated, declines moreslowly than in comparable environments withuniform conditions of growth. We presume that thisimplies a higher level of genetic variance in hetero-geneous environments at mutation–selection equi-librium, although we have not found a formaltreatment of this situation.


Fig. 6 History of B–lines. Each plotted point is a spore.

In a previous experiment (Bell, 1997), linesdescending from a genetically diverse base popula-tion retained higher levels of genetic variance infitness when cultured in a heterogeneous environ-ment than when cultured in a uniform environment.In this case, conditions of growth in the hetero-geneous environment differed with respect to theconcentrations of macronutrients in minimal media.The effect was attributed to the slower eliminationof variance under less intense directional selection,primarily because there was no difference betweentreatments with and without deliberate site-specificdensity-regulation. In the present experiment, therewas no deliberate attempt to impose local density-regulation (within the Light and Dark flasks), butthe effect cannot be explained merely from theslower elimination of variance in heterogeneousenvironments, because there was no genetic vari-ance, or very little, present in the founding popula-tions. We suggest that local density-regulation wasinadvertently imposed by our experimental design:in batch culture, growth is inevitably limited to someextent by the density of cultures within flasks. Itremains conceivable that the quantity of variance inan initially clonal population eventually tends to anequilibrium under mutation–selection balance, andthat this equilibrium is higher in a heterogeneousenvironment because directional selection is weaker.However, this seems much less plausible when, as inthe present case, genotypes that are distinctlyspecialized for light or dark growth arise during thecourse of the experiment, rather than being merelyretained from an initially diverse stock. The mosteconomical interpretation of our results seems to bethat a cost of adaptation, demonstrated by the anti-clinal response of lines initially unable to grow wellin Dark conditions, generates negative frequency-


dependent selection through the limitation of popu-lation growth within flasks, leading to the evolutionof higher levels of genetic variance in the sympatriclines.

The effect is quite modest. The variance of thesympatric populations exceeds, on average, that ofeither allopatric population; but it does not equalthat of the combined allopatric populations. This isbecause the massive immigration implied by mixingand redistributing the cultures in each generationcounteracts the effect of selection. Morepronounced specialization might be displayed ifmigration were restricted.

Genetic variance is markedly greater in the Light,but not in the Dark. This would follow if selection inthe Light against spores selected in the Dark is lessintense than selection in the Dark against sporesselected in the Light; as is probably the case. Thissuggests the general rule that in a heterogeneousenvironment genetic variance will be greater in morepermissive and less in more restrictive habitats.

Acknowledgements

This work was funded by a Research Grant from theNatural Sciences and Engineering Research Councilof Canada. X.R. was supported by a PostdoctoralFellowship from the Ministere de la Recherche etde la Technologie, France. We are grateful to LoriPilkonis for technical assistance, and to ArnoldBennett for critical comments on an earlier draft.

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