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Reticulate Evolution and Taxonomic Concepts in the Ranunculus

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Reticulate Evolution and Taxonomic Concepts in the Ranunculus TAXON • 16 September 2009: 22 + 1 pp. Hörandl & al. • Evolution in the Ranunculus auricomus complex Reticulate evolution and taxonomic concepts in the Ranunculus auricomus complex (Ranunculaceae): insights from analysis of morphological, karyological and molecular data Elvira Hörandl1,2, Johann Greilhuber1, Katarina Klímová2, Ovidiu Paun3, Eva Temsch1, Khatere Emadzade1 & Iva Hodálová4 1 Department of Systematic and Evolutionary Botany, University of Vienna, Rennweg 14, 1030 Vienna, Austria. [email protected] (author for correspondence) 2 Regional Association for Nature Conservation and Sustainable Development Šancova 96, 831 04 Bratislava 3, Slovakia 3 Jodrell Laboratory, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, U.K. 4 Institute of Botany, Slovak Academy of Science, Dúbravská cesta 14, 845 23 Bratislava, Slovakia The Ranunculus auricomus complex is an interesting model system for studying the evolution and diversity of apomictic polyploid complexes. It comprises hundreds of agamospecies, usually referred to two distinct mor- photypes (traditionally named “R. auricomus” and “R. cassubicus”) which are connected by several intermedi- ate forms. Here we try to elucidate the evolution of apomictic “cassubicus” morphotypes and we test criteria for different classification concepts by combining the information of molecular phylogenetic, morphological, karyological and population genetic data (AFLPs, amplified fragment length polymorphism). Phylogenetic analysis based on sequences of the nrDNA ITS and plastid data (matK, trnk, psbJ-psbA) suggest a deep split between the diploid sexual species R. notabilis (“auricomus” morphotype) from the closely related allopatric taxa R. cassubicifolius and R. carpaticola (“cassubicus”). The apomictic “cassubicus” morphotypes are not monophyletic, as one, R. hungaricus, groups with R. notabilis, which may be due to hybrid origin. Morphometric studies and ploidy level determinations via Feulgen densitometry show a transition from 4x R. hungaricus to the 6x apomictic hybrid derivatives of R. cassubicifolius and R. carpaticola. In two accessions, AFLPs and flow cytometric data suggest local gene flow among different apomictic polyploid morphotypes. Frequent facultative sexuality of apomicts may increase genetic diversity by continuous formation of new cytotypes, local hybridization and introgression, which obstructs the fixation of distinct agamospecies. We conclude that “R. cassubicus” and “R. auricomus” cannot be regarded as species but should be treated as either informal groups, or as (notho)taxa at the sectional level. To reflect the different evolutionary processes involved, we propose a separate classification of the sexual species, R. notabilis and the closely related species pair R. cas- subicifolius and R. carpaticola. Based on these well-defined biological species, the apomictic biotypes can be classified as nothotaxa. KEYWORDS: apomixis, Europe, molecular systematics, morphometry, Ranunculus auricomus agg., taxonomy in Antennaria (Bayer & Chandler, 2007) and in Boechera INTRODUCTION (Koch & al., 2003). Studies on population genetics have Apomictic polyploid complexes offer challenging shown that apomictic complexes harbour considerable questions for evolutionary research and classification. genetic diversity within and among populations (review in Apomixis, a mode of reproduction via asexually formed Hörandl & Paun, 2007). Pollen usually remains functional seed (Asker & Jerling, 1992; Richards, 2003), leads to in these lineages and functionality is reduced by meiosis the stabilization and dissemination of single genotypes. and the occurrence of facultative sexually reproducing Apomictic lineages were traditionally thought to be ge- individuals has been demonstrated in several apomictic netically invariant lineages that originated from hybrid- complexes (Asker & Jerling, 1992). In fact, backcrossing ization and polyploidization of sexual species that later of apomictic individuals with sexual individuals, hybrid- became fixed by apomixis (e.g., Stebbins, 1950). Hybrid ization between apomictic lineages and facultative sexual- origin and highly complex and reticulate relationships ity within populations are, along with mutations, the main within apomictic groups have been confirmed by molecu- factors promoting the recurrent formation of new geno- lar studies, e.g., in Hieracium s.l. (Fehrer & al., 2007a, b), types (Hörandl & Paun, 2007). Non-maternal offspring 1 Hörandl & al. • Evolution in the Ranunculus auricomus complex TAXON • 16 September 2009: 22 + 1 pp. may also arise from a partial expression of the apomictic areas (Hörandl & Paun, 2007). Within the genus Ranuncu- developmental pathway. Apomixis usually requires the lus, this complex has sometimes been treated as a separate coordination of embryo sac development without meiosis section because of the great diversity of morphotypes, (apomeiosis) and the development of the egg cell without cytotypes and ecotypes that it contains (Borchers-Kolb, fertilization (parthenogenesis). Uncoupling of these pro- 1983; Loos, 1997) and the ca. 800 microspecies that have cesses leads to shifts in the ploidy levels of the offspring been described (Hörandl & Gutermann, 1998a). (Nogler, 1984a). Thus, meiosis plus parthenogenesis re- Due to its high levels of diversity, the R. aurico- sults in a dihaploid offspring (n + 0); meiosis plus fertiliza- mus complex has often been subdivided into four mor- tion results in a homoploid recombined offspring (n + n, phological groups (auricomus, cassubicus, fallax and BII hybrids) and fertilization of an apomeiotic egg cell monophyllus sensu Hörandl & Gutermann, 1998a) or results in an increase in ploidy level (2n + n, BIII hybrids). corresponding morphological grades, i.e., “morphologi- From these processes, apomictic lineages with vary- cal expressions” (Ericsson, 1992, 2001). Two of the most ing levels of stability and possessing distinct morpho- common morphotypes have frequently been classified logical, ecological and geographical features have origi- as R. cassubicus L. s.l. and R. auricomus L. s.l. Follow- nated in many genera. If such lineages are recognised ing the suggestion of Ericsson (2001), these names are as (agamo)species, apomicts would constitute half of the used in quotation marks throughout this paper to des- species diversity of the flora of the British Isles (Richards, ignate the traditionally recognized morphotypes. These 2003). The abundance and wide distribution of agamic morphotypes show striking differences in leaf shape. complexes, as observed in, e.g., dandelions (Taraxacum The “R. cassubicus” morphotypes possess basal sheaths spp.), blackberries (Rubus fruticosus agg.) and hawkweeds without leaf blades (cataphylla) and large undivided basal (Hieracium s.l.; see Hörandl, 2006a; Van Dijk, 2003), leaves, while stem leaves may be broad or divided into raises the need for practicable taxonomic concepts for segments with a smooth or toothed margin. The “R. au- biodiversity research and flora writing. Not only do apo- ricomus” morphotypes lack basal sheaths and are char- mictic complexes have a reticulated evolutionary struc- acterized by the presence of heterophyllous leaves. Basal ture, meaning that it is difficult to assign their position leaves can be deeply divided while stem leaves are linear in hierarchical classifications, such complexes are also with predominantly entire segments. The basal leaves not equivalent to biological species because of the lack of of the “auricomus” and the “cassubicus” morphotypes interbreeding between populations. Furthermore, they are are not homologous because they arise from different often too diverse to be regarded as ecological units. Con- shoot systems (Hörandl & Gutermann 1998a; Lohwasser, sequently, apomictic complexes are often treated as infor- 2001) and morphological diversity is further increased mal groups such as aggregates (agg.) (sensu Ehrendorfer, by specific features of the torus (Borchers-Kolb, 1983, 1973; Stace, 1998) or often simply called “complexes” 1985; Hörandl & Gutermann, 1998a). The broad series (e.g., Grant, 1981). Within complexes, the formal clas- of intermediate morphotypes between the “cassubicus” sification of “microspecies” or “agamospecies” has been and “auricomus” morphotypes have often been summa- applied to apomictic lineages with a morphological and rized under the names R. fallax (Wimm. & Grab.) Slob. ecological distinctiveness comparable to that exhibited by and R. monophyllus Ovcz., though some authors have sexual species (e.g., Stace, 1998). Application of agamo- treated these four main morphotypes as formal species species concepts requires internal constancy and stability and have assigned distinct populations to subspecies (e.g., of the apomictic lineage(s) both spatially and temporally Marklund, 1961, 1965). The impossibility of demarcating (Weber, 1995, 1996; Hörandl, 1998). Understanding the clear boundaries between the four main morphotypes has evolutionary history, the extent of residual sexuality and encouraged most authors to abandon Marklund’s concept the extent of internal stability of apomictic lineages is and adopt a microspecies concept for those groups of therefore essential for a practicable taxonomic concept. populations that are morphologically distinct (Ericsson, The Ranunculus auricomus complex (R. auricomus 1992; Hörandl, 1998). agg.) is an interesting model system for studying the dy- Most of the polyploid cytotypes of the R. auricomus namics of evolution
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