Ecological and Evolutionary Opportunities of Apomixis

Publishedonline 16 May 2003

Ecologicaland evolutionar yopportunitiesof apomixis: insightsfrom Taraxacum and Chondrilla

Peter J.van Dijk NetherlandsInstitute ofEcology (NIOO-KNAW), Centre for Terrestrial Ecology, Boterhoeksestraat 48, 6666 GA Heteren, TheNetherlands ([email protected] ) The ecological andevolutionary opportunitiesof apomixis in theshort and the long term are considered, basedon two closely related apomictic genera: Taraxacum (dandelion)and Chondrilla (skeletonweed). In both genera apomicts have awidergeographical distribution than sexuals,illustrating theshort-term ecological successof apomixis. Allozymes andDNA markers indicatethat apomictic populations are highly polyclonal. In Taraxacum,clonal diversity canbe generated by rare hybridization betweensexuals and apomicts,the latter acting aspollen donors.Less extensive clonal diversity is generatedby mutations within clonal lineages.Clonal diversity may bemaintained by frequency-dependentselection, caused by biological interactions(e.g. competitors and pathogens). Some clones are geographically widespreadand probably representphenotypically plastic ‘general-purposegenotypes’ . The long-term evolutionary successof apomictic clonesmay belimited by lack ofadaptive potential andthe accumulation ofdeleterious mutations. Although apomictic clonesmay beconsidered as ‘ evolutionary deadends’ , thegenes controlling apomixis canescape from degenerationand extinction via pollen in crossesbetween sexuals and apomicts. In this way,apomixis genesare transferredto a new geneticbackground, potentially adaptive andcleansed from linked deleteriousmutations. Consequently, apomixis genescan be much older than theclones they are currently containedin. The closephylogenetic relationship between Taraxacum and Chondrilla andthe similarity oftheir apomixis mechanismssuggest that apomixis in thesetwo genera couldbe of common ancestry. Keywords: asexual; geographical parthenogenesis;clonal diversity; mutation accumulation; ancientasexuals

1. INTRODUCTION cal andevolutionary opportunitiesof apomixis will be illustrated by twoclosely related genera with apomixis in Apomixis is asexual reproductionthrough seeds.Gameto- theAsteraceae family (Compositae),namely Taraxacum phytic apomixis hasbeen reported in 140 angiosperm gen- (dandelion)and Chondrilla (skeletonweed). It will be era (Carman 1997), suggesting that this form ofapomixis argued that thesuccess of apomicts in thelong run has arisen many timesin thehistory ofthe angiosperms. dependscritically ontheir ability tocrosswith sexual rela- It isgenerally acceptedthat apomixis canflourish over tives andthat this enablesapomixis tosurvive muchlonger shorttime-scales. Theoretically, adominantapomixis time periodsthan generally thought. genewould spread to fixation in anoutcrossing population ofhermaphrodites (Charlesworth 1980; Marshall & Brown1981). 2. APOMIXISIN TARAXACUM AND CHONDRILLA However,apomixis has notplayed animportant role in The genera Taraxacum and Chondrilla are speciesaggre- theevolution of the angiosperms. It has notled to exten- gates,variable in breeding system,ploidy level anddegree sive radiation; it has beenestimated that only onein 1000 ofreproductiveisolation. They are perennial hemicrypto- angiosperm speciesis apomictic (Mogie 1992). There are phytesbelonging tothe tribe ofthe Lactuaceae. Taraxa- nocompletely apomictic genera in theangiosperms cum is foundin disturbedgrounds, meadows and woods (Stebbins1950). Phylogenetically, apomixis has a‘twiggy’ throughout Europe(Richards &Sell 1976; figure 1). distribution.Extant apomicts always have closely related Chondrillajuncea occursin dry openhabitats, andhas a sexual taxa, andcan often be crossed with these,apomicts southerndistribution in Europe;northwards into northern acting aspollen donors.Darlington (1939) andStebbins France andsouthern central Russia(Iljin 1930; Sell 1976; (1950) argued that apomixis has limited evolutionary figure 2). Both genera also occurin Asia andmay have potential andthat apomicts are doomedto early extinc- their origin in theHimalayas (Richards 1973). The weedy tion. dandelionshave beenintroduced by humansin all conti- In this article, theshort-term andthe long-term ecologi- nents,with theexception of Antarctica. Chondrilla is intro- ducedin Australia, andNorth andSouth America. The mostobvious morphological differencesbetween One contribution of 21to a DiscussionMeeting Issue ‘Mechanisms Taraxacum and Chondrilla are theshape of the scape and regulating gene flow inflowering plants’. theinflorescence (capitulum). The scapein Taraxacum is

Phil. Trans. R.Soc.Lond. B (2003) 358, 1113–1121 1113 Ó 2003 TheRoyal Society DOI10.1098/ rstb.2003.1302 1114P. J.van Dijk Apomixis in Taraxacum and Chondrilla

Figure 1. Thegeographical distribution of sexual and apomictic typesin theweedy dandelions ( Taraxacum section Ruderalia) in Europe, basedon Menken et al. (1995). Thedashed line indicates thenorthern distribution limit of apomictic dandelions, thedotted line thatof thesexual dandelions. Note thatwithin thesexual range apomicts also are found. Thedistributions of sexual and asexual typesin thesouth of Europe are not sufficiently known.

Figure 2. Thegeographical distribution of sexual and apomictic typesin Chondrilla in Europe, basedon chromosome numbers published in Goldblatt &Johnson (1978 –2000), Poddubnaja-Arnoldi (1933), Chaboudez (1994) and Chaboudez &Burdon (1995), assuming thatdiploids are sexuals and triploids are apomicts. Thedashed line indicates thenorthern distribution limit of apomictic Condrilla,thedotted line therange of thesexual Chondrilla.Diploids belong to thespecies C.pauciflora (= C.urumoffii ) and C.chondrilloides. non-branched,without leaves; that of Chondrilla is The basic chromosomenumber in Chondrilla is five, in branchedwith leaves.The capitulum of Taraxacum is Taraxacum eight. Sexuals are always diploid ( Chondrilla: large (100–200 florets),solitary andterminal, whereasthat 2x = 10; Taraxacum: 2x = 16) andare generally self- of Chondrilla is small (9–12 florets)terminal, lateral or incompatible (Poddubnaja-Arnoldi1933; Okabe 1956). auxillary, andsometimes produced in groups (Richards & Apomictsare always polyploids, commonly triploid Sell 1976; Sell 1976). The fruitsare achenes(single- (Chondrilla: 3x = 15; Taraxacum: 3x = 24). Apomixis seededfruits), with along rostrum andpappus, providing involves meiotic diplospory: arestitutionnucleus is pro- highly effectivedispersal by wind(Sheldon & Burrows ducedduring meiosisI, followedby anormal meiosisII 1973). Taraxacum and Chondrilla are phylogenetically (Bergman 1950; Nogler 1984). Of thetwo resulting unre- closely related,based on morphology (Bremer 1994) and ducedmegaspores onedegenerates and the surviving chloroplast DNA restriction sitevariation (Whitton et al. unreducedmegaspore formsan unreduced embryo sac 1995). with anunreduced egg cell.This unreducedegg cell then

Phil.Trans. R. Soc.Lond. B (2003) Apomixis in Taraxacum and Chondrilla P.J.van Dijk 1115 developsparthenogenetically intoan embryo. The endo- environmental hypothesesand may also reflectidiosyn- sperm developswithout fertilization, directly from the cratic historical colonization patterns. central cell nucleus(autonomous endosperm develop- Humanintroductions of weedy dandelions to North ment). Most Taraxacum apomicts are obligate apomicts, America andof skeleton weed to America andAustralia butfacultative or partial apomixis, with somesexual seed always involve apomicts,suggesting that theseindeed are set,has also beenreported (Richards 1973). bettercolonizers than sexuals. Chondrilla has become a seriousweed of cereal cultivations in Australia andis a target for biological control(Burdon et al. 1981). 3. THE GEOGRAPHICALDISTRIBUTION OF Becauseapomixis isintimately associatedwith poly- SEXUALSAND APOMICTS ploidy it is possiblethat theunderlying causefor geographical parthenogenesisis primarily adifferencein Figure 1showsthe geographical distributionsof sexual ploidy level, rather than adifferencein breeding system andapomictic weedydandelions in Europe.Figure 2 (Bierzychudek 1987). Differentgeographical distributions showsthe same for skeletonweed. The general picture is betweendiploids andpolyploids are also oftenobserved clear: apomicts have amuchwider distribution in both in strictly sexual plant species(Stebbins 1950; Van Dijk genera. In Taraxacum,apomicts dominatethe northern et al. 1992). regions; in Chondrilla,apomicts dominatethe western and easternparts. The distributions,however, are notpara- 4. CLONALDIVERSITY patric; in large parts sexualsand apomicts canbe found growing together.Different geographical distributionsof Allozyme, andmore recentlyDNA marker, studieshave sexualsand parthenogens are commonin animals and demonstratedthat apomictic Taraxacum and Chondrilla plants (Bell 1982; Bierzychudek 1987); this phenomenon populations are highly polyclonal within their native range. is knownas geographical parthenogenesis(Vandel 1928). Atthe smallest scale,within sites(such as pastures, In Europe, Taraxacum showsa more orlessclassic north – meadowsand roadsides) many clonesco-occur. Menken polyploid, south –sexual contrastof geographical partheno- et al. (1995) reportedbetween 7 and16 clonesin 11 pas- genesisand a similar north –southcontrast occurs in turesamples in Taraxacum in westernand central Europe, Taraxacum in Japan (Morita 1976). in thearea wheresexuals and apomicts are sympatric Several hypotheseshave beenput forward toexplain the (sample sizebetween 14 and79 plants per population). tendencyfor asexuals tooccur farther tothenorth in the Becauseonly fourpolymorphic allozyme loci wereused, Northern Hemisphere.It hasbeen suggested that asexuals this is likely tobe an underestimationof the number of are confinedto environments with limited biotic interac- clones.Van derHulst et al. (2000) applied AFLP markers tions(Levin 1975; Glesener& Tilman 1978; Bell 1982). toestimate clonal diversity in Taraxacum in meadowsin In theseregions apomicts couldreplace sexualsowing to The Netherlandsand Denmark, respectively, 150 and their intrinsic reproductiveadvantage; however,in areas 750 km north ofthe nearest known sexual population, and with complex communities,sexuals would dominate between28 and34 differentAFLP genotypeswere found becausethey cankeep up the coevolutionary arms race in sample sizesranging from 61 to65 plants. with antagonistsor becausesexuals are betterin filling The patternsof clonal diversity foundin Chondrilla narrow andspecialized niches.Another hypothesis resemblethose found in Taraxacum.High clonal diver- assumesthat temporally varying environmentsselect more sitieswere found in 16 purely apomictic populations in effectively for phenotypically plastic genotypes ‘general- westernTurkey (Chaboudez& Burdon1995). In small purposegenotypes ’ in apomictic populations than in sex- samplesof 17 individual plants per site,the number of ual populations.Apomicts could therefore occupy more genotypesranged from 2to11, basedon 8 polymorphic extreme andfluctuating, marginal environments(Lynch loci. In aregional study,sampling 123 apomictic Chond- 1984). Alternatively, Peck et al. (1998) pointedout that rilla populations with 1plant per population in central interbreeding with maladapted immigrants erodeslocal Turkey, 6polymorphic loci distinguished91 clones adaptation in sexual populations,which createsan advan- (Chaboudez1994). However,only 3cloneswere detected tage for asexual reproduction.Therefore asexuals are in 23 populations in southeastAustralia, where Chondrilla more likely toreplace sexualswhen local productivity is wasintroduced from Europeat thebeginning ofthe twen- lowand immigration ratesare relatively high, which is the tieth century,indicating astrong foundereffect casein thenorthern regions ofthe Northern Hemisphere. (Chaboudez1994). Whereasthe hypotheses outlined above relate geo- Mostgenotypes in thesestudies were confined to a graphical parthenogenesisto environmental heterogeneity, single population, butwidespread clones have beenfound it may also beexplained by differenthistorical colonization in both genera.One six-locus Chondrilla genotypewas patterns.Apomictic populations may have expandedmore spreadover more than 700 km in easternTurkey rapidly from therefuges at theend of the Pleistocene than (Chaboudez& Burdon1995), andVan derHulst et al. sexual populations (Stebbins1950), autonomousapo- (2000) reportedtwo AFLP typesoccurring in aDutch micts, like Taraxacum and Chondrilla,canstart anew anda Danish meadow,separated by 600 km. Widespread population from asingle colonist,whereas sexual outcros- cloneshave also beendetected by allozyme studiesin non- sersneed at least twocolonists. The twocentres of sexual weedy Taraxacum (Van Oostrum et al. 1985; Battjes et al. dandelionsin Europe(see figure 1) couldreflect expan- 1992). Suchwidespread clones are probable candidates sionfrom an Iberian anda Balkan Pleistocenerefuge at for general-purposegenotypes, as they will experiencea theend of thePleistocene. The non-classicwest –central– widerange ofenvironments. Their widedistribution must eastcontrasts in Chondrilla are difficult toexplain by the have beenachieved over many generationsby winddisper-

Phil.Trans. R. Soc.Lond. B (2003) 1116P. J.van Dijk Apomixis in Taraxacum and Chondrilla sal andbecause of the relatively small sample sizesin stud- part ofthe niche occupied by thesexuals. Interclonal iesso far, andthe high clonal diversities in populations, selectionbetween clones with overlapping nicheswill it isunclear whether widespread clones are commonin resultin apartitioning ofthe ecological space. Chondrilla and Taraxacum. Various studieshave indicatedthat coexisting Taraxa- cum clonesare ecologically differentiated.As early as 1928, Sukatschewexperimentally demonstratedthat three 5. WHAT CAUSESCLONAL DIVERSITY? dandelionclones that co-occurredin ameadownear St Clonal diversity may bedue to: (i) mutationswithin Petersburg reacteddifferently with respectto density asexual lineages,generating satellite clones;or (ii) crosses, andintraspecific competition (Sukatschew1928). Similar generating daughter clones.Mutations in asexual lineages experiments wereconducted by Solbrig &Simpson(1974, may comprise ‘normal’ mutations(e.g. substitutions, 1977) showingthat coexisting clonesdiffered in repro- chromosomal rearrangements) andthe products of ductivecapacity andresponse to competition anddisturb- autosegregation (Gustafsson1947 a;Richards 1996 a). ance.In transplant experiments,Vavrek et al. (1996) Chromosomal rearrangements may causeposition effects, demonstratedthat eight coexisting clonesdiffered in their suchas silencing ofgenes. Examples ofautosegregation seasonaldevelopment, resulting in differencesin compe- are theloss of chromosomes because of incomplete tition capacity from other plant species.Over thewhole nuclearrestitution or becauseof anaphase bridges,leading year therewere no differences in fitnessbetween these todisomics (3 x 2 1 (Sørensen& Gudjonsson1946)). clones,but phenological differentiation promotedclonal Autosegregation may also bedue to crossing-over during coexistence(Vavrek et al. 1996, 1998). diplospory, resulting in homozygosity at thechromosomal In Taraxacum little is knownabout theeffect of patho- regions distal tothe crossover (Darlington 1939). King & genson the clonal structureof populations.However, the Schaal (1990) reportedmutations at ribosomal DNAand rust fungus Puccinia chondrillina has beenused for biologi- alcohol dehydroxygenase loci in apomictic progeniesof cal controlof Chondrilla in Australia (Burdon et al. 1981). Taraxacum. Mes et al. (2002) foundAFLP, allozyme and The introductionof Puccinia causeda shift in thefre- microsatellite variation within awidespreadNorth Euro- quencyof thethree Chondrilla clones:one sensitive clone peanclone in the Taraxacum section Naevosa. decreasedbut two others increased in frequency.In Tur- In general, thechanges caused by mutation will be key,within thenative range ofapomictic Chondrilla, the small. Muchlarger changesinvolve theformation ofnew mostfrequent clones in populations wereover-infected by daughter clonesvia hybridization, andbecause Chondrilla Puccinia (Chaboudez& Burdon1995). In adetailedstudy and Taraxacum are hermaphrodites, apomicts canact as ofone Turkish population, Espiau et al. (1998) detected pollen donorsin crosseswith facultative apomicts and eight differentresistance phenotypes among 19 Chondrilla with sexuals.A part ofthe progeny in suchcrosses is plants andseven Puccinia pathotypes among 15 isolates apomictic (Richards 1973; Tas &Van Dijk 1999). (Espiau et al. 1998). Suchbiotic interactionshave the In regions wheresexuals and apomicts are sympatric, potential toaffect clonal diversity. The distribution of Tar- crossesbetween sexuals and apomicts cangenerate new axacum and Chondrilla clonesin populations is typically apomictic clones.In purely apomictic regions newapom- L-shaped,with afewcommon and many rare clones ictic clonescan arise locally in crossesbetween facultative (Chaboudez& Burdon1995; Menken et al. 1995). This apomicts;however, facultative apomixis in Taraxacum is may bethe result of frequency-dependent selection, driven rare andthe probability ofeuploid offspring in across by biotic interactions. betweentwo triploids is very low.Perhaps it ismore likely that clonesin thepurely apomictic regions originated in 7. THEFUTUREOF CLONES theregions wheresexuals and apomicts are sympatric and have spreadsince then. The occurrenceof widespread The occurrenceof widespreadclones in thenative range clones in Taraxacum and Chondrilla indicatesthat clones andthe successful introduction to other continentsillus- candisperse over large distancesover time. Stebbins trate theecological successof apomictic clonesin Chond- (1950) has suggestedthat if newclones arise via crosses rilla and Taraxacum:clearly in theshort term apomixis can in sympatric ranges,clonal diversity will decreasefurther besuccessful. In thelong term, however,asexual lineages away from thesexual regions.In Taraxacum high levels of are consideredas evolutionary deadends (Darlington clonal diversity are still foundin Denmark, at 750 km 1939; Maynard Smith 1978; Judson& Normark 1996). north ofthe nearest known sexual population (Van der Onereason for their early extinction may bethat clones Hulst et al. 2000). This clonal diversity may representa cannotadapt well tochanging environments,because they dynamic equilibrium betweenimmigration ofnewly lack geneticvariation. The rate ofadaptation dependson formedclones from thesouth and local extinction ofold thelevel ofgenetic variation. This may beespecially clones,due to evolutionary processesdiscussed below. important in thecoevolutionary arms race with pathogens (theRed Queen hypothesis (Hamilton 1980; Bell 1982)), asillustrated by the Chondrilla–Puccinia studiesmen- 6. ECOLOGICALDIFFERENTIATION BETWEEN tionedabove. CLONES Anotherfactor that may contributeto theearly extinc- Newclones can only establish whenthey findan empty tionof clones is degenerationdue to an increasing niche,different from thoseoccupied by thesexuals and mutation load.Muller ’sratchet isthe idea that theclass theother clones.According to the ‘frozenniche variation ’ with fewestslightly deleteriousmutations gets lost by model(Vrijenhoek 1984), apomixis fixes only asmall part chancein small asexual populations (Muller 1964). This ofthe sexual genepool andtherefore freezes only asmall classis then lost forever, because it cannotbe recreated

Phil.Trans. R. Soc.Lond. B (2003) Apomixis in Taraxacum and Chondrilla P.J.van Dijk 1117

A S

r A S

r A S S r A

clone 1 clone 2 time clone 3 clone 4 clone 5

Figure 3. Schemeshowing how an apomixis gene (dominant A)can move to agenomic background of arecent sexual history viaintrogression. For simplicity adiploid witha single chromosome is indicated. Theintensity of theshading of the chromosomes indicates thelength of theasexual history. Newclones arise through crosses between sexuals and apomictic pollen donors. Thearrow withS represents achromosome drawn from thesexual gene pool. Thearrow with ‘r’ indicates a crossover during pollen meiosis in theapomictic clone. Owing to repeated backcrossesand crossing over, theregions closely linked totheapomixis gene (A) will havea longer asexual history than therest of thegenome of theclone and will accumulate deleterious mutations over multiple clonal generations. by recombination asit canin asexual population. Rep- 8. ANCIENTAPOMIXIS GENES etition ofthis processleads to a gradual accumulation of slightly deleteriousmutations in asexual lineages,which Apomixis in Taraxacum is controlledby twodominant couldeventually lead toextinction. When the genomic loci: onefor unreducedegg cells(diplospory) andone for mutation rate for mildly deleteriousmutations is higher parthenogenesis(Richards 1973; Van Dijk et al. 1999; Van than oneper generation,mutations will also accumulate Dijk &Bakx-Schotman 2003). Whena newapomictic deterministically in large asexual populations (Kond- cloneis formedin acrossbetween a sexual andan apom- rashov 1982). If mildly deleteriousmutations interact syn- ictic pollen donor,the apomixis geneswill move toa new ergistically, they will notaccumulate in sexual populations geneticbackground. This newgenetic background can becausethese mutations can be effectively purged.The potentially beadaptive andprovides newopportunities for Ysexchromosomes of mammals andplants are thebest theapomixis genes,when the environment is changing examples ofdegeneration in theabsence of recombination (Mogie 1992). (Rice1996; Charlesworth &Charlesworth 2000; Charles- Becausethe maternal genomeof the new apomictic worth2002). In thelong run,a similar degenerationpro- cloneis drawnfrom asexual genepool, this genomewill cessis expectedto occur in apomictic lineages. belargely freedfrom deleteriousmutations. In anewtrip- The factthat apomicts are polyploids has consequences loid cloneonly oneof the three genomes will bederived for mutation accumulation:(i) themutation rate per indi- from thesexual genomepool; however, repeated vidual will beenhanced; and (ii) theeffects of deleterious backcrossingover several clonal generationswill resultin mutationswill bebetter masked by wild-type alleles. This theintrogression ofthe apomixis genesinto thesexual will resultin thebuild-up of a higher mutation load in geneticbackground. The apomixis genesbecome associa- polyploids than in diploids.Accumulation of deleterious tedwith genomeswith lowgenetic loads. Crossing over mutationsin asexuals isinevitable, butpolyploidy will during pollen meiosiswill also remove linked deleterious slowdown the rate ofdegeneration. mutationson the chromosomes on which theapomixis Unfortunatelythere are noreliable age estimatesof Tar- alleles are located.This processis illustrated in figure 3. axacum clones.Based on their wideand disjunct geo- Meanwhile,the original clonesin which theapomixis graphical distribution,Gustafsson (1947 b)assumedthat geneswere contained may degenerateowing toaccumu- certain microspeciesin Taraxacum couldbe more than lation ofdeleterious mutations and eventually become 100 000 years old.Menken et al. (1995) foundthat sexual extinct. andapomictic dandelionsshared the major allozyme poly- For sucha cleansing cycleto work, the frequency of morphisms, andthat null andprivate alleles in triploid backcrossingshould be sufficiently high compared with apomicts wererare. This suggestsa recentorigin ofthese therate ofdeleteriousmutation accumulation.Moreover, clones,at least notolder than afewmillion years. it will workonly in crossesbetween sexuals and apomicts,

Phil.Trans. R. Soc.Lond. B (2003) 1118P. J.van Dijk Apomixis in Taraxacum and Chondrilla

Scolymus are responsiblefor thenon-transmission of apomixis genes via haploid pollen grains. This is what is expectedto hap- Hymenonema penaccording tothe introgression schemein figure 3. As Rothmaleria theprobability ofacrossoverbetween two loci is positively Catananche correlated with their physical distance,chromosomal regions closeto the apomixis geneshave alowerprob- Cichorium ability ofbecoming cleansed.Therefore, deleterious Stephanomeria mutationsare expectedto accumulate over clonal gener- ationsaround apomixis genes.Consistent with this expec- Crepis tation,microsatellite markers that are linkedto the Taraxacum diplospory locusin Taraxacum showsevere segregation Chondrilla distortionin haploid pollen grains, butnot in diploid pol- lengrains (P.J.van Dijk, unpublishedresults). Lactuca Agoseris 9. THE FUNCTIONOF POLLENIN TARAXACUM Pyrrhopappus AND CHONDRILLA Mostapomictic speciesare pseudogamous,meaning Sonchus that pollen is necessaryfor fertilization ofthe central Dendroseris nucleusin order todevelop endosperm. Pollen, however, Hieracium has nofunction for seedproduction in autonomousapo- micts like Taraxacum and Chondrilla.Amutation causing Tolpis male sterility has nonegative effecton seed fertility. On Malacothrix thecontrary, if resourcesno longer neededfor pollen pro- ductioncould be allocated toseed production, such a Hedypnois mutation wouldincrease fertility. Functionlesscharacters Hyoseris are expectedto degenerate over time. Nevertheless,more Leontodon than 80% ofall British Taraxacum microspeciescontinue toproduce pollen (Richards 1986) andin addition they Hypochaeris producefunctionless yellow petals andmost of them nec- Scorzonera tar. Accordingto Maynard-Smith (1978, p.41) ‘it is diffi- cultto suggest any explanation ofthese facts, other than Tragopogon that theseclones may berelatively recentin origin, and Figure 4. Thetaxonomic distribution of various typesof that evolutionary adaptation in asexual populations is apomixis in thetribe of Lactuceae (Asteraceae), basedon slow,so that maladapted featuresare retained ’. themorphological phylogeny of Bremer (1994). Apomixis However,pollen productionmakes sense in thelight of wasnot included in thecladistic analysis. Theblack circles newclone formation. Male-sterile clonescannot generate indicate meiotic diplospory, thegrey circle indicates mitotic newapomictic daughter clonesin crosseswith sexuals. diplospory and theopen circles indicate apospory. Suchmale-sterile clonesmay becomeextinct through insufficientadaptability or an increasing mutation load. Only pollen-fertile apomicts canproduce new daughter andnot in crossesbetween two facultative apomicts.In clones,which will theninherit thepollen functionfrom thelatter casethe new apomictic lineage will inherit the their apomictic fathers(Mogie 1992). Not only domost mutational loadsof the two apomictic parental lineages. apomictic dandelionsproduce pollen, pollen meiosisis in Isthere any indication for ahigh mutation load in Tar- general also reductional,in contrastto female meiosis, axacum?In sporophytic polyploid tissuerecessive deleteri- which is restitutional (diplospory). Clonesproducing only ousmutations will bemasked by wild-type alleles. unreducedpollen grains are knownin Taraxacum However,recessive lethals will becomeexpressed in hap- (Richards 1973) andin Chondrilla (Bergman 1950), but loid pollen grains whenapomictic triploids are crossed are notcommon. A reductionalmale meiosismakes sense with diploid sexuals.In crossesbetween diploid sexual and in thelight ofnewclone formation: adiploid pollen grain triploid apomictic Taraxacum significantly fewerdiploid from atriploid apomict producesa newtriploid apomict hybrids than triploid hybrids have beenreported, suggest- in acrosswith asexual diploid. Anunreduced triploid ing that haploid pollen indeedis less viable than diploid pollen grain, however,would result in anewtetraploid pollen (Morita et al.1990; Tas &Van Dijk 1999). apomict in sucha cross.With unreducedpollen meiosis Nogler (1984) has suggestedthat apomixis genesare eachnew clonal generation wouldhave anelevated ploidy recessivelylethal in pollen grains andthat thereforeapo- level compared with theprevious one.Such lineages mixis genescan be transmitted only in aheterozygous would ‘polyploidize themselvesout of existence ’ (Stebbins statein diploid pollen,but not in ahomozygous statein 1950, p.389) andbecome extinct. haploid pollen.This couldexplain why diploidy and gametophytic apomixis in general are incompatible. How- ever,apomixis genesin Taraxacum are dominant,not 10. THEEVOLUTIONOF MEIOTICDIPLOSPORY IN recessive(Richards 1973; Van Dijk &Bakx-Schotman THE ASTERACEAE 2003). Richards (1996 b)has suggestedthat it isnot the The primary evolutionof the meiotic diplospory type of apomixis genesthemselves but linked recessivelethals that apomixis is likely tobe a rare event,because at least two

Phil.Trans. R. Soc.Lond. B (2003) Apomixis in Taraxacum and Chondrilla P.J.van Dijk 1119 mutationsmust be combined that individually are del- (Lindb. fil.) Dahlst.from Czechoslovakia. Bot. Jahr.Syst. eterious.Diplospory alonegenerates offspring with 114, 315–328. increasing ploidy levels,which will polyploidize itself out Bell, G.1982 The masterpiece ofnature: the evolution and genetics ofexistence within afewgenerations; however, partheno- ofsexuality .Berkeley, CA:University of California Press. genesisalone generateshaploid offspring with lowfitness. Bergman, B.1950 Meiosis in two different clones of theapomictic Chondrilla juncea . Hereditas 36, 297–320. Consequently,strong selectionis expectedagainst these Bierzychudek, P.1987 Patterns in plant parthenogenesis. In individual mutationsand the chances that thesemutations The evolution ofsex and its consequences (ed. S.C.Stearns), are simultaneouslypresent in apopulation, andwill be pp. 197–217. Basel, Switzerland: Birkha¨user. combinedby intercrossing,are very remote. Birky Jr, C.W.1996 Heterozygosity, heteromorphy, and However,when apomixis genescan continuously move phylogenetic trees in asexual eukaryotes. Genetics 144, tonew adaptive andclean genetic backgrounds, apomixis 427–437. genescould thus survive long periodsof time andcan be Bremer, K.1994 Asteraceae. cladistics and classification . Port- ancient.Bergman (1950) statedthat ‘therestitution mech- land: Timber Press. anism in Taraxacum correspondsin all essentialswith that Burdon, J.J., Groves, R.H.&Cullen, J.M.1981 Theimpact of Chondrilla’.Couldapomixis in thesetwo genera have a of biological control on thedistribution and abundance of commonancestry? Figure 4showsthe occurrence of mei- Chondrilla juncea in southeastern Australia. J.Appl. Ecol. 18, otic diplospory plottedon a morphological phylogeny of 957–966. Carman, J.G.1997 Asynchronous expression of duplicate theLactuceae tribe. This showsthat meiotic diplospory is genes in angiosperms maycause apomixis, bispory, tetras- clusteredwithin thesubtribe oftheCrepidineae, to which pory, and polyembryony. Biol. J.Linn.Soc. 61, 51–94. also Ixeris,athird genuswith meiotic diplospory, belongs Chaboudez, P.1994 Patterns of clonal variation in skeleton (Nogler 1984; Carman 1997). Accordingto the phy- weed (Chondrilla juncea ),an apomictic species. Aust.J. Bot. logeny, commonancestry of meiotic diplospory in Taraxa- 42, 283–295. cum, Chondrilla and Ixeris is apossibility. Alternatively, Chaboudez, P.&Burdon, J.J.1995 Frequency dependent meiotic diplospory in thesegenera evolved independently selection in awild plant –pathogen system. Oecologia 102, threetimes, implying apredispositionfor theevolution of 490–493. meiotic diplospory in thesubtribe ofthe Crepidineae. Charlesworth, B.1980 Thecost of sexin relation to mating Commonancestry of apomixis in Taraxacum and Chon- system. 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B., Hasan, S.&Chaboudez, P.1998 Host –pathogen diver- Recently,it has beensuggested that thedivergence sityin awild system: Chondrilla juncea–Puccinia chondrillina . betweenalleles at alocuscan be used for theestimation Oecologia 113, 133–139. ofclonal age (Birky 1996; Judson& Normark 1996). Glesener, R.R.&Tilman, D.1978 Sexuality and thecompo- Owing togenetic drift, ASD in asexual population is nents of environmental uncertainty: clues from geographic restricted,whereas ASD in anasexual organism is,in prin- parthenogenesis in terrestrial animals. Am. Nat. 112, 659– ciple, unlimited (Birky 1996). Onthe basis ofASD, 673. Lahn& Page (1999) wereable todetect four episodes of Goldblatt, P.&Johnson, D.1978 –2000 Index to plant chromosome numbers1975– 1997. Monographsin systematic botany suppressionof recombination onthe human X-chromo- fromthe MissouriBotanical Garden ,vol. 5,8,13, 23, 30, 40, some.Using ASD, Welch &Meselson(2000) have pro- 51, 58, 69 and 81. 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Phil.Trans. R. Soc.Lond. B (2003) Apomixis in Taraxacum and Chondrilla P.J.van Dijk 1121 logeny ofapomixis. Are youfamiliar with any studiesin Have interploidy crossesbetween sexual 2 x and Nx plants which apomixis has beenmapped ontophylogenies? beendone, and what dothey tell usabout imprinting in P.J.van Dijk. Iam notaware ofany attempts tocon- Taraxacum? ductthis type ofstudy but it wouldbe valuable. (Loren P.J.van Dijk. Diploid –tetraploid crosseshave been Reisberg pointedout a studythat heand a studenthad made in the1940s and1950s by various people,all indi- publishedin AmericanJournal of Botany in whichapomixis cating that 3 x plants are easyto obtain in either cross wasmapped ontoa phylogeny.) direction.Moreover, Brink andCooper have shownthat R.Vinkenoog ( Departmentof Biology and Biochemistry, early embryo growth isindependent of the development University ofBath,Bath, UK ). Anautonomous apomictic ofthe endosperm. This indeedsuggests that thereis no 3x dandeliondevelops a purely maternal endospermwith- (notmuch) imprinting in Taraxacum. outany paternal contribution.How does it overcomethe imprinting problem? Onepossibility is that in Taraxacum GLOSSARY (both sexual andapomictic) thereis no(strong) AFLP:amplified fragment length polymorphism imprinting systempresent. What isknown about this? ASD:allele sequencedivergence

Phil.Trans. R. Soc.Lond. B (2003)