Southern isolation and northern long-distance dispersal shaped the phylogeography of the widespread, but highly disjunct, European high mountain plant Artemisia eriantha (Asteraceae)

We investigated the range dynamics of Artemisia eriantha, a widespread, but rare, mountain plant with a highly disjunct distribution in the European Alpine System. We focused on testing the roles of vicariance and long-distance dispersal in shaping the current distribution of the species. To this end, we collected AFLP and plastid DNA sequence data for 17 populations covering the entire distributional range of the species. Strong phylogeographical structure was found in both datasets. AFLP data suggested that almost all populations were genetically strongly differentiated, with 58% of the overall genetic variation partitioned among populations. Bayesian clustering identified five groups of populations: Balkans, Pyrenees, Central Apennines, one southwestern Alpine population and a Widespread cluster (eastern Pyrenees, Alps, Carpathians). Major groups were supported by neighbor-joining and NeighbourNet analyses. Fourteen plastid haplotypes were found constituting five strongly distinct lineages: Alps plus Pyrenees, Apennines, Balkans, southern Carpathians, and a Widespread group (eastern Pyrenees, northern Carpathians, Mt. Olympus). Plastid DNA data suggested that A. eriantha colonized the European Alpine System in a westward direction. Although, in southern Europe, vicariant differentiation among the Iberian, Italian and Balkan Peninsulas predominated, thus highlighting their importance as glacial refugia for alpine species, in temperate mountain ranges, long-distance dispersal prevailed. This study emphasizes that currently highly disjunct distributions can be shaped by both vicariance and long-distance dispersal, although their relative importance may be geographically structured along, for instance, latitude, as in A. eriantha. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174, 214–226.

[1]  C. R. Hobbs,et al.  Asian origin and upslope migration of Hawaiian Artemisia (Compositae–Anthemideae) , 2013 .

[2]  P. Schönswetter,et al.  Quaternary range dynamics of ecologically divergent species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan refugium , 2011 .

[3]  X. Fang,et al.  Origin and development of Artemisia (Asteraceae) in Asia and its implications for the uplift history of the Tibetan Plateau: A review , 2011 .

[4]  K. Winker,et al.  Discord reigns among nuclear, mitochondrial and phenotypic estimates of divergence in nine lineages of trans‐Beringian birds , 2011, Molecular ecology.

[5]  P. Schönswetter,et al.  The wide but disjunct range of the European mountain plant Androsace lactea L. (Primulaceae) reflects Late Pleistocene range fragmentation and post‐glacial distributional stasis , 2010 .

[6]  P. Schönswetter,et al.  Bayesian hypothesis testing supports long-distance Pleistocene migrations in a European high mountain plant (Androsace vitaliana, Primulaceae). , 2009, Molecular phylogenetics and evolution.

[7]  M. Brändle,et al.  Pleistocene phylogeography and phylogenetic concordance in cold‐adapted spring snails (Bythinella spp.) , 2009, Molecular ecology.

[8]  P. Schönswetter,et al.  Genetic structure of peripheral, island-like populations: a case study of Saponaria bellidifolia Sm. (Caryophyllaceae) from the Southeastern Carpathians , 2009, Plant Systematics and Evolution.

[9]  K. Marhold,et al.  Contrasting phylogeographies inferred for the two alpine sister species Cardamine resedifolia and C. alpina (Brassicaceae) , 2009 .

[10]  H. John B. Birks,et al.  Alpines, trees, and refugia in Europe , 2008 .

[11]  Orr Spiegel,et al.  Mechanisms of long-distance seed dispersal. , 2008, Trends in ecology & evolution.

[12]  P. Schönswetter,et al.  Historical divergence vs. contemporary gene flow: evolutionary history of the calcicole Ranunculus alpestris group (Ranunculaceae) in the European Alps and the Carpathians , 2008, Molecular ecology.

[13]  L. Excoffier,et al.  The Hidden Side of Invasions: Massive Introgression by Local Genes , 2008, Evolution; international journal of organic evolution.

[14]  M. Ronikier,et al.  High genetic differentiation in the alpine plant Campanula alpina Jacq. (Campanulaceae): evidence for glacial survival in several Carpathian regions and long‐term isolation between the Carpathians and the Alps , 2008, Molecular ecology.

[15]  G. Schneeweiss,et al.  Molecular phylogeny and evolution of floral characters of Artemisia and allies (Anthemideae, Asteraceae): evidence from nrDNA ETS and ITS sequences , 2008 .

[16]  J. Tyráček Quaternary Glaciations—Extent and Chronology, Part I: Europe, J. Ehlers, P.L. Gibbard (Eds.). Elsevier, Amsterdam (2004), 488pp., €185, USD 210, GBP 123.50, ISBN: 0-444-51462-7 , 2008 .

[17]  P. Taberlet,et al.  Genetic structure of Hypochaeris uniflora (Asteraceae) suggests vicariance in the Carpathians and rapid post‐glacial colonization of the Alps from an eastern Alpine refugium , 2007 .

[18]  M. Hoffmann,et al.  PARALLEL EVOLUTIONARY PATTERNS IN MULTIPLE LINEAGES OF ARCTIC ARTEMISIA L. (ASTERACEAE) , 2007, Evolution; international journal of organic evolution.

[19]  P. B. Eidesen,et al.  Nuclear vs. plastid data: complex Pleistocene history of a circumpolar key species , 2007, Molecular ecology.

[20]  S. Giménez Una aproximació a l'estudi de l'evolució i la sistemàtica en "Artemisia" i gèneres afins en els àmbits de la filogènia i citogenètica moleculars , 2007 .

[21]  Noah A. Rosenberg,et al.  CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure , 2007, Bioinform..

[22]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[23]  Heidi M. Meudt,et al.  Almost forgotten or latest practice? AFLP applications, analyses and advances. , 2007, Trends in plant science.

[24]  H. Comes,et al.  Long-distance dispersal vs vicariance: the origin and genetic diversity of alpine plants in the Spanish Sierra Nevada. , 2006, The New phytologist.

[25]  D. Ehrich aflpdat: a collection of r functions for convenient handling of AFLP data , 2006 .

[26]  D. Huson,et al.  Application of phylogenetic networks in evolutionary studies. , 2006, Molecular biology and evolution.

[27]  Mattias Jakobsson,et al.  The Pattern of Polymorphism in Arabidopsis thaliana , 2005, PLoS biology.

[28]  Laurent Excoffier,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[29]  P. Taberlet,et al.  How to track and assess genotyping errors in population genetics studies , 2004, Molecular ecology.

[30]  Michael P. Cummings,et al.  PAUP* [Phylogenetic Analysis Using Parsimony (and Other Methods)] , 2004 .

[31]  Jukka Corander,et al.  BAPS 2: enhanced possibilities for the analysis of genetic population structure , 2004, Bioinform..

[32]  H. Nybom Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants , 2004, Molecular ecology.

[33]  G. Hewitt Genetic consequences of climatic oscillations in the Quaternary. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  Nicholas H. Barton,et al.  The Effects of Genetic and Geographic Structure on Neutral Variation , 2003 .

[35]  John P. Huelsenbeck,et al.  MrBayes 3: Bayesian phylogenetic inference under mixed models , 2003, Bioinform..

[36]  R. Petit,et al.  Glacial Refugia: Hotspots But Not Melting Pots of Genetic Diversity , 2003, Science.

[37]  H. Comes,et al.  Differential cycles of range contraction and expansion in European high mountain plants during the Late Quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae) , 2003, Molecular ecology.

[38]  P. Schönswetter,et al.  Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium Sternb. & Hoppe (Campanulaceae) in the European Alps , 2002, Molecular ecology.

[39]  J. Stewart,et al.  Cryptic northern refugia and the origins of the modern biota , 2001 .

[40]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[41]  K. Crandall,et al.  TCS: a computer program to estimate gene genealogies , 2000, Molecular ecology.

[42]  P. Taberlet,et al.  Genetic diversity in an endangered alpine plant, Eryngium alpinum L. (Apiaceae), inferred from amplified fragment length polymorphism markers , 2000, Molecular ecology.

[43]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[44]  J. Searle,et al.  Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  Yves Van de Peer,et al.  Construction of evolutionary distance trees with TREECON for Windows: accounting for variation in nucleotide substitution rate among sites , 1997, Comput. Appl. Biosci..

[46]  K. Bennett Evolution and Ecology: The Pace of Life , 1996 .

[47]  W. Jordan,et al.  LOW LEVELS OF INTRASPECIFIC GENETIC VARIATION AT A RAPIDLY EVOLVING CHLOROPLAST DNA LOCUS IN NORTH AMERICAN DUCKWEEDS (LEMNACEAE) , 1996 .

[48]  John C. Avise,et al.  Molecular Markers, Natural History and Evolution , 1993, Springer US.

[49]  E. Jäger,et al.  Vergleichende chorologie der zentraleuropaischen flora , 1993 .

[50]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[51]  Ling Yeou-ruenn The Old World Artemisia Linn. (Compositae) , 1992 .

[52]  J. V. Xirau Dades sobre la biologia d'especies iberico-baleariques d'Artemisia L. , 1989 .

[53]  A. Coleman,et al.  Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species , 1988 .

[54]  J. Plaziat Late cretaceous to late eocene palaeogeographic evolution of southwest Europe , 1981 .

[55]  A. Bennett The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[56]  Claudia Baier,et al.  Evolution And Ecology The Pace Of Life , 2016 .

[57]  G. Kozlowski,et al.  Phylogenetics and phylogeography of the monocot genus Baldellia (Alismataceae): Mediterranean refugia, suture zones and implications for conservation. , 2011, Molecular phylogenetics and evolution.

[58]  C. Robinson FAUNA AND FLORA , 2011 .

[59]  B. Erschbamer,et al.  Alpine species seed longevity in the soil in relation to seed size and shape – A 5-year burial experiment in the Central Alps , 2010 .

[60]  Facultat de Farmàcia UNA APROXIMACIÓ A L'ESTUDI DE L'EVOLUCIÓ I LA SISTEMÀTICA D'ARTEMISIA I GÈNERES AFINS , 2007 .

[61]  M. Hershkovitz Ribosomal and chloroplast DNA evidence for diversification of western American Portulacaceae in the Andean region , 2006 .

[62]  J. Shaw,et al.  The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. , 2005, American journal of botany.

[63]  A. de Queiroz The resurrection of oceanic dispersal in historical biogeography. , 2005, Trends in ecology & evolution.

[64]  J. Nylander Bayesian Phylogenetics and the Evolution of Gall Wasps , 2004 .

[65]  M. Calvet The Quaternary glaciation of the Pyrenees , 2004 .

[66]  P. Schönswetter,et al.  Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium in the European Alps , 2002 .

[67]  J. Huelsenbeck,et al.  MRBAYES : Bayesian inference of phylogeny , 2001 .

[68]  E. Mcarthur,et al.  Artemisia systematics and phylogeny: Cytogenetic and molecular insights , 2001 .

[69]  M. P. Cummings,et al.  PAUP* Phylogenetic analysis using parsimony (*and other methods) Version 4 , 2000 .

[70]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[71]  B. Cabezudo,et al.  Libro rojo de la flora silvestre amenazada de Andalucía. I. Especies en peligro de extinción , 1999 .

[72]  H. Piękoś-Mirkowa,et al.  Distribution and habitats of Artemisia eriantha [Asteraceae] in the Tatra Mts [Western Carpathians] , 1998 .

[73]  J. Franco,et al.  Atlas de la flora del Pirineo aragonés , 1997 .

[74]  张荣祖 历史生物地新趋势—分衍生物地理学(Vicariance Biogeography) , 1990 .

[75]  S. Siljak-Yakovlev,et al.  A Propos De La Classification Des Taxons Endemiques Basee Sur La Cytotaxonomie et La Cytogenetique , 1986 .