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Extreme Environmental Change and Evolution: Stress-Induced

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Extreme Environmental Change and Evolution: Stress-Induced Extremeenvironmentalchangea ndevolution: stress-inducedmorphologicalvariationi sstrongly concordantwithpatternsof evolutionarydivergence inshrewmandibles AlexanderV .Badyaev *{ and KerryR. Foresman Division of Biological Sciences,The University of Montana, Missoula, MT 59812-1002,USA Morphologicalstructures oftenconsist ofsimpler traits whichcan be viewed as either integrated(e.g. correlateddue to functional interdependency) or non-integrated (e.g. functionally independent) traits. Thecombination of along-term stabilizingselection onthe entire structure witha short-term directional selection onan adaptively important subset oftraits shouldresult inlong historical persistence of integratedfunctional complexes, with environmentally induced variation and macroevolutionary change con¢ned mostly to non-integrated traits. Weexperimentallysubjected populationsof three closelyrelated species of Sorex shrews toenvironmental stress. Aspredicted, wefoundthat most ofthe variationin shrew mandibularshape was localized between rather thanwithin the functionalcomplexes; the patterns of integrationdid not change between the species. Thestress-induced variationwas con¢ ned to non- integratedtraits andwas highly concordant with the patterns ofevolutionarychange öspecies di¡ered in the same set ofnon-integrated traits whichwere most sensitive tostress withineach species. Wesuggest that lowenvironmental and genetic canalization of non-integrated traits mayhave caused these traits to bemost sensitive notonly to the environmentalbut alsoto genetic perturbations associated with stress. Thecongruence of stress-induced andbetween-species patterns ofvariation in non-integrated traits suggests that stress-induced variationin these traits mayplay an importantrole in species divergence. Keywords: environmentalstress; canalization;functionalintegration ;mosaicevolution; Sorex gration(and the associatedenvironmental canalization) 1.INTRODUCTION canstrongly facilitate adaptive evolution by reducing the Understandingthe evolutionof complex morphological environmentalvariance in each of the integratedtraits structures is acentral questionin evolutionary biology and,thus, minimizingenvironmental variance ortho- (e.g.Bonner 1988; Ra¡ 1996) .Complexstructures often gonalto the adaptivedirection of morphological change consist ofsimpler morphologicaltraits whichcan be forthe entire structure (Lande1 980,1 984;W agner1988) . viewedas either integratedor non-integrated, e.g. func- On the other hand,morphological integration could have tionallyintegrated traits arehighly dependent on each beenproduced by historically invariant developmental other becausethey are involved in the same organismal patterns (e.g.Riedl 1978);the highgenetic canalization of function(such asattachment ofa muscle).Incontrast, integratedtraits canreduce the expressionof genetic non-integratedtraits arefunctionally and developmen- variationand slow or bias morphological responses tothe tallyindependent of each other (reviewedin Cheverud present selection (Lande1 979;Stearns 1993;W agner et al. 1996). 1997). Quantitativegenetics theorypredicts that long-term Attempts toresolve the constrainingand facilitating stabilizingselection andcorrelated mutations will facilitate roles ofintegration have led to the developmentof a integratedtraits evolvinggenetic correlations consistent conceptof mosaic evolution (Simpson 1953; W agner1996) . withtheir functionalor developmental relationships and, Thetheory of mosaic evolution assumes the existence of ultimately,evolvingin a correlatedmanner compared to relativelyindependent morphological units (e.g.functional the more independentevolution of non-integrated traits complexes)within a structure;such relativelyinvariant (Lande1979, 1980; Cheverud 1 982,1984) .Indeed,many complexesare subject toa long-term stabilizingselection studies havedocumented strong in£ uences ofdevelop- whichpreserves the basiclevel of integration necessary mental andfunctional integration on the structure of across environments.Directional selection exerted by phenotypicand genetic covariation (Cheverud ( 1996)and changingenvironments can favour rearrangements of references therein). these complexes,thereby producing changes in the overall However,it is unclearwhether the correlatedevolution structure, whilemaintaining integration within each ofintegratedtraits constrainsor facilitatesadaptive modi- complex.Thus, the combinationof along-term stabilizing ¢cationsof morphologicalcomplexes (reviewed in Arnold selection onthe entire structure withstrong short-term 1992;Wagner et al.1997).On onehand, morphological inte- directionalselection onasubset ofunits withina structure shouldresult inhigher variation between complexes of integratedtraits, but lowervariation within these * Author forcorrespondence (abadyaev@selway .umt.edu). { Present address:331 F unchessHall, Department of Biological complexes(Simpson 1 953;Berg 1960; Cheverud 1 984; Sciences,Auburn University,Auburn, AL36849,USA. Wagner1996; W agner& Alternberg1996). Proc. R.Soc.Lond. B (2000) 267, 371^377 371 © 2000The RoyalSociety Received 2September1999 Accepted 1November1999 372A. V.Badyaevand K. R.Foresman Stress and mosaic evolution Here wetest twopredictions of the mosaictheory of (untreated)plots and plots where the overstorey vegetation was evolution.First, persistent stabilizingselection on removed.W edesignedour study within theseplots to minimize complexesof integrated traits favourslow sensitivity of thee¡ ects of immigration and emigration following treatments the integratedtraits toenvironmental and genetic pertur- (seeBadyaev et al. (2000)for details of theexperimental design bations(i.e. environmentaland genetic canalization; andtrapping schedules) .The vegetationremoval treatment Schmalhausen1 949;Cheverud 1 982;W agner1988; createshighly stressful conditions for shrews, as evidenced by Wagner et al. 1997).Highcanalization of integrated largeincreases in thedevelopmental instability of shrew complexesreduces the heritablephenotypic variation embryosand by a decreasein theindividual conditions of adults availableto natural selection and,thus, canlead to low (Badyaev et al. 2000).Weexamined56 0two-to three-month- rates ofevolutionarychange within integrated complexes. oldindividuals of threeclosely related Sorex species(F umagalli et Thus,we can predict alonghistorical persistence of al. 1999;see F oresman( 1999)for details of the species biology): complexesof integrated traits (Lande1979; BjÎ rklund Sorexcinereus (control,46 males and 43 females, and vegetation 1994)and high similarity ofrecently divergedspecies in removal,74 males and 44 females) , Sorexmonticolus (control,37 integratedtraits (Wagner1 988;Schluter 1996 a). On the malesand 37 females, and vegetation removal, 39 males and 38 contrary,non-integratedtraits whichare relatively free of females)and Sorexvagrans (control,46 males and 52 females, persistent stabilizingselection maybe less environmen- andvegetation removal, 46 males and 58 females) .All sex- tallyand genetically canalized (Stearns &Kawecki1994; relatedvariation was removed from the data in generallinear Stearns et al. 1995).Thisshould lead to greater variability modelsand standardized residuals were used for all analyses. innon-integratedtraits inresponse toboth environmental Leftand right shrew mandibles were positioned on a slide andgenetic perturbations and to faster evolutionin these andthen photographed under 7.5magni¢ cation using an £ traits (Wagner1996; W agner et al. 1997).Thus,we can OlympicSZH stereo photomicroscope and a videocapture predict that recently divergedspecies shouldbe the most board.The resultingimages were further magni¢ ed 2 using £ di¡erent innon-integrated traits. Second,if lower envir- MochaImage Analysis software ( JandelScienti¢ c) .The data onmentalcanalization of non-integrated traits is asso- were the x- and y-coordinatesof 1 7homologousmorphological ciatedwith their lowergenetic canalization (Gavrilets & landmarks(¢ gure 1 a).Instudies such as ours, the variance Hastings 1994;W agner et al. 1997),then the variation resultingfrom the positioning of amandibleunder a microscope betweenrecently divergedspecies shouldbe similar tothe istypically much higher than the variance from repeated environmentallyinduced variation within each species ö measuresof already scanned images. Thus, we usedthe reposi- species shoulddi¡ er the most inthe same traits that are tioningerror as ameasurementerror term in ouranalysis. Each the most sensitive toenvironmental variation within mandiblewas repositioned and digitized three times. High species. magni¢cation and three replicates for each measure allowed us Threeclosely related species of Sorex shrews providea tominimize and estimate the measurement error. Repeated goodsystem inwhich to examine these predictions measureswere separated by several measurement sessions. Both experimentally.First, existingwork on the anatomyof the mandiblephotography (by a laboratorytechnician) and mand- shrew mandibleallowed us toassign mandibular areas a iblemeasurements by A. V.B. wereconducted without prior priori tointegrated (i.e. participatingin the attachment of knowledgeof the treatment, sex or species of the measured the same muscle) andnon-integrated units (e.g.Kindahl animal.Thus, we assumedthat the measurement error contrib- 1959;DÎ tsch 1982).Second,previous work on the sensi- utedequally to each treatment category . tivityof the shrew mandibleto environmental conditions Todescribethe functional integration in theshrew mandible,
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