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Ecological and Evolutionary Opportunities of Apomixis

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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 eco- logical 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 ‘ evol- utionary 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 has beenreported 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 times in thehistory ofthe angiosperms. dependscritically ontheir ability tocrosswith sexual rela- It is generally 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 an important role in The genera Taraxacum and Chondrilla are speciesaggre- theevolution ofthe angiosperms. It has notled to exten- gates,variable in breeding system,ploidy level anddegree sive radiation; it has beenestimated that only onein 1000 ofreproductive isolation. 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 unreducedembryo sac 1995). with an unreducedegg 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). better colonizersthan 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 is intimately associatedwith poly- SEXUALSAND APOMICTS ploidy it is possiblethat theunderlying causefor geo- graphical 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 recently DNA 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). At thesmallest 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
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