EDAPHIC DIFFERENTIATION IN : A MODEL FOR STUDIES IN EVOLUTIONARY ECOLOGY Author(s): Nishanta Rajakaruna Source: Madroño, Vol. 50, No. 1 (JANUARY-MARCH 2003), pp. 34-40 Published by: Botanical Society Stable URL: http://www.jstor.org/stable/41425490 . Accessed: 18/10/2013 21:05

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This content downloaded from 68.189.1.182 on Fri, 18 Oct 2013 21:05:19 PM All use subject to JSTOR Terms and Conditions Madroño,Vol. 50, No. 1, pp. 34-40, 2003

EDAPHIC DIFFERENTIATION IN LASTHENIA : A MODEL FOR STUDIES IN EVOLUTIONARY ECOLOGY

Nishanta Rajakaruna Departmentof Biological Sciences, 371 Serra Mall, StanfordUniversity, Stanford,CA 94305-5020 nishanta@ stanford.edu

Abstract Thecurrent knowledge of thegoldfield Lasthenia is discussed,emphasizing the possible role of edaphicfactors in thedivergence of thispredominantly Californian genus. Lasthenia occupy a widearray of edaphic ranging from serpentine outcrops to saltflats to guano deposits, thriving underspecific ion and osmotic conditions that are uninhabitable forthe vast majority ofspecies. Studies showthat ion accumulation and sequestration are commonstrategies used to counterosmotic effects, commonto mosthabitats harboring Lasthenia species. Inter- and intra-specific variation in toleranceto edaphicconditions has been observed in closely related yet reproductively isolated taxa, suggesting that edaphicfactors may have set the stage for the diversification ofthis genus. Lasthenia provides numerous opportunitiestoexamine the link between adaptation, reproductive isolation and speciation. KeyWords: adaptive divergence; California flora; edaphic races; Lasthenia ; salinity tolerance; serpentine.

Accordingto Lindleyand Moore (1876), "they 1989; Desrochersand Böhm 1993) to assess bio- ( Lasthenia) growin wet places,and appearto be systematicrelationships and determinetrends of uninterestingweeds." Theydo "growin wetplac- biochemicalevolution in thegenus. Electrophoretic es," but studiesof Lasthenia(: Astera- workfollowed to establishevolutionary relation- ceae) overthe last severaldecades have shownthe shipsamong closely related taxa withinthe genus genus to consistof anythingbut "uninteresting(Crawford et al. 1985;Crawford and Ornduff 1989) weeds." Commonlyknown as goldfields, of as well as withinthe highly variable L. californica Lastheniaoccupy large areas of the Californian land- sensuOrnduff (Desrochers and Böhm 1993).More scape,casting spectacular carpets of brightly-colored recently, comprehensive phylogenetic studies goldenyellow flowers in earlyspring. A recentmo- (Chan et al. 2001, 2002; Desrochersand Dodge lecularphylogenetic study recognized 21 speciesand 2003) havecontributed to ourunderstanding ofpat- subspeciesbelonging to sevensections (Chan et al. ternsof divergencein Lasthenia.The studyby 2001). All butone speciesare endemicto theCali- Chan et al. (2001) agreeswith observations made fornianFloristic Province. Lasthenia kunthii (Less.) earlier(Ornduff 1966, 1976) thatdivergence pat- Hook & Arn.,the only member of thegenus found ternsin thegenus conform to expectationsof cat- outsidewestern , is endemicto vernal astrophicselection and saltationaldiversification pools and wetlandsin centralChile (Ornduff 1966). (Lewis 1962). Membersof thegenus have wideedaphic tolerance Existingknowledge suggests that Lasthenia can andare found in habitatssuch as coastalbluffs, gua- providea modelsystem for studies in evolutionary no deposits,vernal pools, salt and alkalineflats, ser- ecology,specifically, in understandingthe role of pentineoutcrops, deserts, grasslands, and open edaphicfactors in differentiation.Species of Las- woodlands(Ornduff 1966, 1993). Membersof L. theniahave successfullycolonized diverse habitats californica sensu Ornduff (Ornduff 1993) have the withinCalifornia, including those that exclude the widestedaphic tolerance within the genus, with pop- vast majorityof species (Ornduff1966, 1993; ulationsspanning all but guano habitats.Keck Kingsburyet al. 1976;Vasey 1985; Rajakaruna and (1959) statedthat L. californica sensu Ornduff [then Böhm 1999; Noe and Zedier 2000; Parsonsand Baeria chrysostoma(Fischer & C. Meyer) E. Whelchel2000). Further,in some sections(e.g., Greene]was themost abundant composite in Cali- sect.Hologymne [Battling] A. Grayand sect.Orn- fornia.Other Lasthenia taxa have ratherrestricted duffia R. Chan)all speciesoccupy the same edaphic distributions,with seven taxa now listedin Califor- habitatyet generally do notgrow intermixed (Orn- nia NativePlant Society's "Inventory of Rare and duff1966), whilein others(e.g., sect. Ptilomeris EndangeredPlants of California"(CNPS 2001). [Nutt.]Ornduff), species occupy contrasting edaph- Following Ornduff's extensive monograph ic habitats(Crawford et al. 1985; Vasey 1985). (1966), Lastheniahas receivedconsiderable atten- Thusit is plausibleto hypothesizethat edaphic fac- tion.Early studies examined inter- and intra-specif- tors may have playedan importantrole in thedi- ic variationin flavonoidchemistry (Saleh and versificationof thegenus. In thispaper, taxa in sev- Böhm1971; Ornduffet al. 1973,1974; Böhm et al. eral sectionsare discussedwith emphasis on the

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possiblerole of edaphicfactors in theirdiversifi- and L. gracilis,suggesting that racial features may cation.Since manyendemic species of flowering have evolved secondarilyin responseto edaphic plantsin westernNorth America are edaphicen- factors(Rajakaruna et al. in pressa). demics(Kruckeberg 1969, 1986),studies of a mod- Recenteco-physiological studies (Rajakaruna et el genussuch as Lastheniacould providegeneral al. 2003) indicatethat race A plantsfrom both L. insightsinto speciation in a varietyof othersuch californicasubsp. californicaand L. gracilisare edaphicallydiverse genera. clearlymore tolerant of potentially-toxicNa+, sug- gestingthat physiological traits responsible for Na+ Lastheniasect. Amphiachaenia (DC.) R. Chan: uptakeand sequestrationmay have evolvedinde- L. californicasensu Ornduff pendentlyin populationsbelonging to the two closelyrelated taxa. Schat et al. (1996) provideone Lastheniasect. Amphiachaenia, formerly known of thebest examples of parallelgenotypic changes as L. sect. Baeria (Fisch. & Mey.) Ornduff,was in toleranceto an edaphicextreme within a recentlyrevised (Chan 2001) to includefour spe- species.Their studies have shownthat loci confer- cies,L. californicaDC. ex Lindl,[consists of subsp. ringcopper tolerance have evolvedindependently californica,subsp. macrantha (A. Gray)R. Chan, in geographicallyisolated populations of Silene vul- and subsp.bakeri (J. T. Howell)R. Chan],L. grac- garisGarcke (Caryophyllaceae). In Plantago(Plan- ilis (DC.) Greene,L. ornduffiiR. Chan,and L. lep- taginaceae),the vacuolar Na+/H+ antiporter activi- talea (A. Gray)Ornduff. and ty,thought to confertolerance to Na+ (Apse et al. L. graciliswere previously recognized as L. cali- 1999) is onlypresent in thesalt-tolerant P. mariti- fornicasensu Ornduff (1993). The twocryptic taxa ma L. butnot in theglycophytic P. mediaL. (Staal foundwithin L. californicasensu Ornduff, L. cali- et al. 1991).This difference is thoughtto be crucial fornica subsp. californicaand L. gracilis,have in theecological divergence of thesetwo species. been the subjectof intenseecological and evolu- Sodiumis clearlyan importantelement in manyof tionarystudies (Rajakaruna and Böhm 1999; Chan the habitatswhere race A is found.Whether the et al. 2002; Desrochersand Dodge 2003). presence/absenceor levelof expressionof theNa+/ A biosystematicstudy (Desrochers and Böhm H+ antiportergene is responsiblefor the differences 1995) firstsuggested the existenceof two geo- in uptakeand accumulationin race A plantsis an graphicalraces within L californicasensu Ornduff area worthyof investigation.Ion uptakestudies based on flavonoidpigments (Böhm et al. 1989; conductedon thetwo races from Jasper Ridge also Desrochersand Böhm 1993), allozymebanding indicatethat race A is moretolerant of highexter- patterns,and cypsela characteristics.A detailed nal Mg2+and low Ca2+/Mg2+ratios (Rajakaruna et ecologicalstudy (Rajakaruna and Böhm 1999) sug- al. 2003). Bothof thesetraits have adaptivesignif- gestedthat the two races describedby Desrochers icance in magnesium-richserpentine and coastal and Böhm(1995) occurin distinctsets of habitats habitatswhere race A is found.The traitsthat have thatcan be classifiedon thebasis of ionic stresses been studied(Na+, Mg2+,Ca2+/Mg2+) are common and wateravailability. Race A plantspredominate featuresin mosthabitats where race A is found, in habitatssubject to ionicstress. Although the soils thus,it is temptingto hypothesizethat differential in theseenvironments are ionicallyharsh, the per- responseto edaphicstresses may have playedan centclay contentis generallyhigh, increasing the importantrole in the racial divergenceof L. cali- waterholding capacity of thesoil. Plantsare often fornicasensu Ornduff.By extendingeco-physio- restrictedto moistor even saturatedsoils in such logicalstudies to characterizethe physiology of hy- environments.In contrast,race С plantsare found bridsbetween the two species (and races),it is pos- in ionically"benign" inland environments.The sibleto appreciatebetter the role of edaphicfactors soils are oftensandy, rocky, and shallow,drying in diversification. out earlyin thegrowing season. The conditionsat The findingsfrom ecophysiological studies (Ra- JasperRidge Biological Preserve (Stanford Univer- jakarunaet al. 2003) suggesta correlationbetween sity,San MateoCo., CA), wherethe races occur in flavonoiddifferences, edaphic features, and ion ac- parapatry,mirror the trends seen acrossthe range cumulation,suggesting a previouslyunknown of thetaxa, with the two races occupyingdistinct adaptiverole for flavonoid differences. The primary microhabitats:Race A occupyingthe wet, yet ion- featurethat distinguishes the edaphicraces in L. ically harshsoils at the bottomof the serpentine californicasubsp. californica and L. gracilisis the ridge,while race С occupiesthe fast-drying,yet flavonoidpigment profile; race A containssulfated ionicallyless stressfulupper reaches (Rajakaruna compounds,namely sulfated kaempferol and quer- and Böhm 1999). At JasperRidge, race A plants cetindiglycosides plus prominenteriodictyol gly- belongto L. californicasubsp. californicawhile cosides (Böhm et al. 1974, 1989; Desrochersand race С plantsbelong to L. gracilis.However, the Böhm 1993) notfound in raceС plants.Ecological racesdo notalways correspond to thetwo taxa rec- rolesfor flavonoid pigments have oftenbeen pos- ognizedby Chan et al. (2001,2002). A recentstudy tulated(Böhm 1987),and thecase fora correlation showsthat one or bothedaphic races have evolved with habitatand sulfatedflavonoids has been in parallelin bothL. californicasubsp. californica broughtforward (Harborne 1975). A largenumber

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of taxa foundin habitatswith water logged and ifornicasubsp. californicaplants; the patternis salineconditions contain sulfated flavonoids (Har- maintainedin the greenhouse.Germination tests borne1975; Barronet al. 1988). In L. californica also revealedevidence for reduced hybrid fitness. subsp. californicaand L. gracilis, sulfatedflavo- Strongecological selection at thesite (Rajakaruna noids occuronly in Na+-accumulating plants that and Böhm 1999) may severelylimit introgression. predominatein ionically-stressedenvironments. It The fateof any hybridsproduced is unknown.A is possiblethat sulfation of flavonoidsmay be ben- transplantstudy of hybridsin parentalhabitats eficialin sulfate-richenvironments where race A would shed lighton possiblepost-zygotic mecha- occurs.Thus, Rajakaruna et al. (2003) hypothesized nismsof isolation.Further studies are neededto an edaphically-linkedecological role for the fla- clarifythe roles of ecologicalselection versus re- vonoiddifferences that first suggested the existence inforcementon the patternsof reproductiveisola- of thesetwo races (Böhmet al. 1974, 1989). tionobserved between races and the two cryptic A studyon theresponse to waterstress suggests planttaxa. thatthe two races from Jasper Ridge show different An understandingof the relationshipbetween life historystrategies in responseto waterstress traitsfor adaptationand reproductiveisolation is (Rajakarunaet al. in pressb). Race С plants(L. criticalto furtherthe hypothesis of edaphicdiffer- gracilis) adopta droughtavoidance strategy often entiationin L. californicasubsp. californica and L. referredto as phenologicalescape (Fox 1990;Aron- gracilis.Studies suggest that reproductive isolation son et al. 1992) and have significantlygreater rela- can be achievedas a by-productof a physiological tivefitness than race A plantsunder increasing water adaptationto unusualsoil conditions(Macnair and stress.In contrast,race A plants(L. californica Gardner 1998). Macnair and colleagues have subsp. californica) adopt a slow-growingstrategy shownthat the linkage block associatedwith cop- and allocatemore biomass to rootthan shoot. This per tolerancein Mimulusguttatus Fischer ex DC. strategyis commonlyseen in herbaceousannuals (Scrophulariaceae)also produceshybrid inviability; growingunder edaphic stress, specifically under wa- however,it is unclearif inviabilityis achievedvia terand nutrient stresses (Kramer 1980; Grime 1994). pleiotropyor hitchhiking.Nevertheless, their work Since the studywas conductedin pottingsoils, to has clearlydocumented that natural selection for an seekeffects of waterstress in isolation,it is unclear adaptivetrait (copper tolerance) has causeda gene how thefindings relate to conditionsexperienced in for post-zygoticisolation to spread throughthe thefield. A large-scaleexperiment using natural soils population(Macnair and Christie1983; Christie is requiredto clarifyfurther the relationship between andMacnair 1987). Whethersuch relationships ex- ionic strength,water availability and fitnesswithin ist betweenedaphic tolerance and observedrepro- environments,and to furtherexplore factors that af- ductiveisolation in L. californicasensu Ornduff is fectthe distribution of theseraces at JasperRidge worthyof investigation. andacross the species' range. Given our understand- ing of the environmentalvariables associated with Lastheniasect. Ptilomeris (Nutt.) Ornduff: differencesin fitness,it is now possibleto conduct L. minorand L. maritima detailedanalysis of selectiongradients (Wade and Kalisz 1990; Dudley1996) to inferthe role of nat- Lastheniaminor (DC.) Ornduffoccurs in a va- uralselection in achievingfitness differences under rietyof habitatssuch as alkaliflats, coastal bluffs, fieldconditions. sanddunes, pond margins, and disturbed sites while Previousstudies (Desrochers 1992) suggested L. maritima(A. Gray)M. Vaseyis restrictedalmost low crossabilityas well as reducedgene flowbe- exclusivelyto islandsand offshorerocks harboring tweenraces (Desrochers and Böhm 1995) ofL. cal- seabirdnesting and roostingsites (Ornduff1965, ifornicasensu Ornduff. A recentstudy using seven 1966;Vasey 1985). The soilson thesesites are high populationsof L. californicasubsp. californica and in nitrogen,low in pH, and highlydisturbed from L. gracilisshow reducedcrossability between the theactivities of thebirds (Vasey 1985). In addition, two closely relatedcryptic taxa (Rajakarunaand constantwind and salt sprayproduce an outright Whittonunpublished). Examination of intra-and hostileenvironment. inter-racialseed set as an effectnested within spe- Ornduff(1966) consideredthe self-compatible L. cies suggeststhat the edaphic races are also repro- maritimato be a recentdescendent from the self- ductivelyisolated. By comparingpatterns of seed incompatibleL. minor.An electrophoreticstudy set withobservations of pollentube growth,it is (Crawfordet al. 1985) furthersupported this hy- clearthat most of thereduction in seed set is due pothesisand suggestedthat speciation probably in- to post-pollination,prezygotic effects. Interestingly, volved a switchto self-compatibility,development thereis evidencefor enhanced prezygotic isolation of autogamy,and subsequentdivergence driven by in theparapatric location at JasperRidge. This pat- edaphicfactors. Given that variation for tolerance ternsuggests a possiblerole forreinforcement in is firstrequired to colonizethe extreme guano hab- the observedisolation. Flowering times have di- itats,it is likelythat self-compatibility arose post- vergedin the parapatriclocation with L. gracilis colonization.Whether the switchto self-compati- plantsalways flowering 7-10 daysprior to L. cal- bilityarose as a by-productof an adaptationto gua-

This content downloaded from 68.189.1.182 on Fri, 18 Oct 2013 21:05:19 PM All use subject to JSTOR Terms and Conditions 2003] RAJAKARUNA:EDAPHIC DIFFERENTIATION IN LASTHENIA 31 no or is directlylinked to a gene conferringadap- vationmade by Ornduff(1966) is thatthese three tationis notknown. closelyrelated species, with edaphic requirements A recentphylogenetic study (Chan et al. 2001) thatappear to be identical,are neversympatric. A showeda close relationshipbetween the two spe- purepopulation of one of thesespecies may exist cies, but it did not conclusivelysupport the pro- withina fewmeters from a purepopulation of an- posed ancestor-descendentrelationship. The close other.Ornduff (1966) attributesthis pattern to oc- relationshipbetween the two species is reflectedby cupationof a site on a "firstcome, firstserved" the high fertilityof artificialcrosses (Ornduff basis, yet admitsthat a detailedecological study 1966). However,Vasey (1985) reportsthat at the probablywould reveal factorsthat are different onlytruly sympatric site known for the two species, amongsuch sites. It is likelythat the threetaxa onlya fewplants appear to be intermediates.Ex- differin theirtolerance regime to edaphicfeatures aminationof parapatricpopulations of thetwo spe- associatedwith salinity. The species-trioprovides cies at threelocalities failed to revealany indication yet anothersetting to explore the relationships of naturalinterspecific hybridization (Vasey 1985). amongadaptation, reproductive isolation, and di- It is possiblethat strong ecological selection is re- versification. sponsiblefor limiting introgression. The physiologicalbasis forthe substratetoler- Lastheniasect. Ornduffia R. Chan: ancein L. maritimais notknown. Preliminary stud- L. fremontii,L. conjugens,and L. burkei ies by Vasey(1985) showthat L. minoris nottol- erantof guano-modifiedsoils. However,it is pos- All threespecies in thissection are inter-cross- sible thatextensive screening may revealtolerant able (Ornduff1966, 1969). The rangesfor L. con- individualsamong populations of this species. Such jugens Greeneand L. fremontii(Torr, ex A. Gray) studiesare criticalto ourunderstanding of theori- Greenemarginally overlap, however, natural hy- gin of L. maritima.Limited work suggests that L. bridsbetween the species are veryrare (Ornduff maritimaaccumulates nitrates in its foliage(Orn- 1969). Artificialhybrids between L. conjugensand duff1965), and Vasey (1985) suggeststhat high L. fremontiishow remarkable similarity to L. burkei nitratecontent in the cells may have allowed L. (Greene)Greene, leading Ornduff (1966) to suggest maritimato growin theseosmotically-challenged a hybridorigin for this taxon. oc- sites. Nitrateuptake has been well characterized cursin vernalpool habitatssimilar to thoseoccu- (Tischner2000), and it is feasibleto determinein pied by itstwo relatives, but its geographical range the laboratorywhether physiological differences is distinct.Many research tools have been utilized existbetween the two speciesin thisregard. Other (Saleh et al. 1971; Crawfordand Ornduff1989; physiologicaldifferences between the two species, Chan et al. 2001) to resolverelationships within suchas toleranceto excesscations such as Na+ and thissection but have notbeen able to supportcon- high osmoticstress, also commonto these sites, clusivelyOrnduff 's hypothesis for the hybrid origin have not been examined.Clearly, there is much of L. burkei. workto be doneto assess mechanismsof tolerance Althoughall threespecies colonize vernal pools, to guanosoils and theL. maritima-L.minor com- theirdistributional pattern within a pool seemsto plex providesan ideal opportunityto do so. Once be relatedto waterlevel, soil moisture,and salinity traitdifferences are establishedbetween the two (Ornduff1966). Ornduff(1966) claimeda similar speciesand theiradaptive significance determined, situation to thatdescribed for the three halophytes it will be possibleto examinetheir genetic basis. in sect. Hologymne,where the species are rarely Whethertraits contributing to adaptationto guano sympatricalthough they may be occupyingsites soils also contributeto isolation(i.e., self-compat-just a fewmeters apart. Again, specific edaphic tol- ibilityor reducedhybrid fitness) can thenbe ex- erancesmay exist among these taxaand amined. the sites theyare restrictedto may in factshow micro-scaledifferences in edaphicfeatures. Only a examinationof these such as our de- Lastheniasect. Hologyme (Battling) A. Gray: close sites, tailed of the at L. chrysantha,L. glabrata, and L. ferrisiae study serpentineoutcrop Jasper Ridge (Rajakarunaand Böhm 1999), will reveal All threespecies in this sectionoccupy saline patternsof soil heterogeneityin theseapparently habitatsand formvigorous, moderate to highlyfer- uniformedaphic habitats. In a studyconducted in tile artificialhybrids (Ornduff 1966). Hybridspe- an artificialvernal pool createdat Berkeley,Orn- ciationwas suspectedin the originof L. ferrisiae duff(1966) demonstratedthat L. conjugenswas al- Ornduff,putatively from hybridization between L. ways restrictedto the soil immediatelyabove and glabrataLindl, subsp. coulteri (A. Gray)Ornduff below the waterlevel whileL. fremontiioccurred and L. chrysantha(Greene ex A. Gray) Greene fromwater level to theupper limit of soil moisture (Ornduff1966). The studyby Chan et al. (2001) (Ornduff1966). Lastheniaconjugens appeared to showminimal molecular variation for species with- be themore water-dependent ofthe two species and in thissection and is uninformativeon thepossible maybe occupyingdeeper vernal pools thatdry out hybridorigin of L. ferrisiae.An interestingobser- laterin thegrowing season. Though physiological

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differencesobviously exist amongthe threespe- studyby Chanet al. (2001) suggeststhat saltational cies, therange of toleranceto salinityand osmotic diversificationhas also occurredin Lasthenia, with effectsis unknown.Characterization of theecolog- a rapidinitial radiation, perhaps into distinct eco- ical amplitudeof thesespecies and theirartificial logicalniches, followed by longperiods of gradual hybridsmay shed light on theimportance of edaph- changepunctuated by renewed,rapid diversifica- ic featuresin thediversification ofthis group. Other tion.Lasthenia has no doubtbeen immenselysuc- species,especially L. kunthii(Less.) Hook andArn. cessfulin adaptingto theecological diversity of its and L. glaberrimaDC. (L. sect.Lasthenia ) are also presentrange similar to otherCalifornian genera restrictedto vernalpools and wetlands,while L. wherecatastrophic selection has supposedlyoper- platycarpha(A. Gray)Greene [L. sect.Platycarpha ated(Lewis 1962; Vargaset al. 1999). (H. M. Hall) Ornduff]is foundpredominately in Edaphicallyrestricted species provide fascinating alkaliflats (Ornduff 1993). examplesfor the studyof plant speciation.The The surveypresented here reveals that the ma- studyof theprocesses leading to theevolution of jorityof Lastheniaspecies are tolerantof unusual suchspecies can shedlight on therelationship be- edaphicconditions, and it is reasonableto suggest tweenadaptation and speciation.With the advent thatthese edaphic features have playedan impor- of genetictechniques such as the studyof quanti- tantrole in thedivergence of thisrelatively small tativetrait loci (QTLs), it is possibleto studycan- genus.Even withinan apparentlyuniform edaphic didate"speciation genes." Perhaps the best-known ,such as a salt flat,populations of differentexample in this regardis in the genus Mimulus speciesare rarelysympatric. This stronglysuggests (Bradshawet al. 1998) wherefloral traits associated thatmicro- scale differencesin edaphicfeatures are withpollinator preference and reproductiveisola- likelyresponsible for their distribution. Although tion have been characterized.This studyimplies species discussedabove are adaptedto deal with thatgenes of largeeffect can contributeto specia- differentspecific ions (e.g., heavymetals, magne- tion.A similarassociation has recentlybeen estab- siumunder serpentine, sodium, magnesium under lishedin Aquilegia(Ranunculaceae) (Hodges et al. saline,nitrate under guano), an importantfactor that 2002). In boththese QTL studies,reproductive iso- is commonto all theseedaphic habitats is thehigh lationis a by-productof adaptationto pollinators, osmoticpressure of thesoil solution.From the in- thusproviding a directlink between adaptation and formationcurrently available for Lasthenia (Orn- speciation. duff1965; Rajakaruna and Böhm 1999; Rajakaruna The genusLasthenia provides numerous oppor- et al. 2003), it appearsthat ion accumulationand tunitiesto examinethe link between adaptation to sequestrationis a commonstrategy used to counter substrateand reproductiveisolation. Many closely thisstress. However, there are inter-and intra-spe- relatedspecies in Lastheniagenerally avoid sym- cificdifferences in mechanismsof toleranceto os- patryand appearto be whollydistinct in areas of moticstress and thesedifferences may have setthe contact.Thus, these species appear to be botheco- stagefor the fascinating ecological divergence seen logicallydivergent and reproductivelyisolated. In in thegenus. Lasthenia, the extent of isolationas well as theex- ManyLasthenia species occur in landthat is geo- tentof ecologicaldifferentiation among closely re- logicallyrather recent, since a largeproportion of latedspecies, has notbeen well documented except theirpresent range was coveredby sea waterduring in thecase of L. califomica sensuOrnduff (Raja- theMiocene and Pliocene(Howard 1951; Axelrod karunaand Whittonunpublished). Traits that are 1956). The inlandsea retreatedat theclose of the associatedwith ecological specialization in closely Pliocene,although saltwater lakes of varying extent relatedspecies can be identifiedand theiradaptive existedin theCentral Valley during the Pleistocene significancecan be demonstrated.If the ecologi- (Flint1947). Some of thelakes and marsheshave cally-divergentspecies are reproductivelyisolated, persistedinto the 19thcentury (Mason 1957) and it will be possibleto examineany linksbetween it is reasonableto speculatethat the ancestorof adaptationto substrateand reproductiveisolation, Lastheniawas tolerantof salinity(specific ion ef- and thus,identify potential "speciation genes." fects)and osmoticeffects. Salinity and osmotic tol- The available phylogeneticinformation (Des- erancemay in factrepresent ancestral traits that rochersand Böhm 1995; Chan et al. 2001, 2002; have been retainedin thevast majority of species Desrochersand Dodge 2003), alongwith the rela- whileit has been lost in a fewothers. Alternately, tively small size of the genus,low base chromo- toleranceto osmoticand salinityeffects may have some number(n = 8), generallyannual habit and independentlyevolved in thevarious species in re- obligatelyoutcrossing nature, and the ease with sponseto theirradiation into unique habitats such whichthe species can be grownfor experimental as vernalpools, alkali flats,serpentine outcrops, studiesmake Lasthenia an ideal modelfor studies and guanodeposits. in evolutionaryecology. The Hawaiiansil vers word alliance (: Madiinae) providesperhaps the most spectacular Acknowledgments and well-studied example of adaptiveradiation in I wishto thankDavid D. Ackerly,Bruce G. Baldwin, plants(Robichaux et al. 1990; Baldwin1997). The SusanP. Harrison,Arthur R. Kruckeberg,and Jeannette

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