BMC Evolutionary Biology | |
The evolutionary history of Antirrhinum in the Pyrenees inferred from phylogeographic analyses | |
Pablo Vargas2  Christophe Thébaud1  Claire Suchet1  Monique Burrus1  Isabel M Liberal2  | |
[1] Laboratoire Evolution et Diversité Biologique (EDB), UMR5174, CNRS - Université de Toulouse (UPS)- ENFA, 118 route de Narbonne, Toulouse, Cedex 9 31062, France;Real Jardín Botánico de Madrid (CSIC), Plaza de Murillo 2, Madrid E-28014, Spain | |
关键词: Quaternary; Pyrenees; Phylogeography; Phylogeny; Antirrhinum; | |
Others : 848401 DOI : 10.1186/1471-2148-14-146 |
|
received in 2014-01-16, accepted in 2014-06-17, 发布年份 2014 | |
【 摘 要 】
Background
The origin and colonisation history after the Quaternary ice ages remain largely unresolved for many plant lineages, mainly owing to a lack of fine-scale studies. Here, we present a molecular phylogeny and a phylogeographic analysis of Antirrhinum, an important model system in plant biology, in the Pyrenees range. Our goal was to reconstruct the evolutionary and colonisation history of four taxa endemic to this region (A. majus subsp. majus, A. majus. subsp. striatum, A. molle, and A. sempervirens) by using a dense sampling strategy, with a total of 452 individuals from 99 populations whose collective distribution spans nearly the entirety of the Pyrenees and adjacent mountains.
Results
Phylogenetic and phylogeographic analyses of the sequences of two plastid (trnS-trnG and trnK-matK) regions revealed the following: (i) historical relationship between the Pyrenees and Iberia (but not with the Alps); (ii) the long persistence of populations in the Pyrenees, at least since the Late Pleistocene; (iii) three different colonisation histories for populations from the Western, Central, and Eastern Pyrenees; (iv) the deep phylogeographic separation of the eastern and western populations; and (v) the colonisation of southern France from the Eastern Pyrenees.
Conclusions
The present study underlines the enormous influence of the glacial history of the mountain ranges on the current configuration of intra- and inter-specific genetic diversity in Antirrhinum, as well as the importance of periglacial areas for the survival of species during glacial periods of the Quaternary.
【 授权许可】
2014 Liberal et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140718071316566.pdf | 2295KB | download | |
Figure 4. | 56KB | Image | download |
Figure 3. | 113KB | Image | download |
Figure 2. | 126KB | Image | download |
Figure 1. | 87KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Varga ZS, Schmitt T: Types of oreal and oreotundral disjunctions in the western Palearctic. Biol J Linn Soc 2008, 93(2):415-430.
- [2]Barthlott W, Mutke J, Rafiqpoor D, Kier G, Kreft H: Global Centers Of Vascular Plant Diversity. Plant Taxonomy to Evolutionary Biology Nova Acta Leopoldina NF 92, Nr 342 2005, 61-83.
- [3]EEA: Biogeographical Regions, Europe 2011. Copenhagen: European Environment Agency; 2011.
- [4]Hewitt G: The genetic legacy of the Quaternary ice ages. Nature 2000, 405(6789):907-913.
- [5]Taberlet P, Fumagalli L, Wust-Saucy A-G, Cosson J-F: Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 1998, 7(4):453-464.
- [6]Schmitt T: Biogeographical and evolutionary importance of the European high mountain systems. Front Zool 2009, 6:9.
- [7]Hewitt G: Genetic consequences of climatic oscillations in the Quaternary. Philos Trans R Soc Lond Ser B Biol Sci 2004, 359(1442):183-195.
- [8]Médail F, Diadema K: Glacial refugia influence plant diversity patterns in the Mediterranean Basin. J Biogeogr 2009, 36(7):1333-1345.
- [9]Hewitt GM: Post-glacial re-colonization of European biota. Biol J Linn Soc 1999, 68(1–2):87-112.
- [10]Dupias G: Végétation Des Pyrénées. Notice Détaillée De La Partie Pyrénéenne De La Carte De La Végétation De La France au 1/200.000e. Toulouse, FR: CNRS; 1985.
- [11]Gómez D, Sesé JA, Villar L: The vegetation of the Alpine Zone in the Pyrenees. In Alpine Biodiversity In Europe. Edited by Nagy L, Grabherr G, Koörner C, Thompson DBA. Berlin, DE: Springer; 2003:85-92. [Ecological Studies no.167]
- [12]Villar L, Dendaletche C: Pyrenees. France, Spain and Andorra. In Centres Of Plant Diversity A Guide And Strategy For Their Conservation. Edited by Heywood VR, Davis SD, Hamilton AC. Cambridge: WWF and IUCN; 1994:61-64.
- [13]Puşcaş M, Choler P: A biogeographic delineation of the European Alpine System based on a cluster analysis of Carex curvula dominated grasslands. Flora Morphol Distrib Funct Ecol Plants 2012, 207:168-178.
- [14]Charlesworth JK: The Quaternary Era: With Special Reference To Its Glaciation. 1957.
- [15]Frenzel B, Pecsi M, Velichko AA: Atlas of the Paleoclimates and paleoenvironments of the Northern Hemisphere. Late Pleistocene Holocene. Gustav Fisher, Budapest 1992.
- [16]Vuia F: Studiul Reliefului Glaciar oei Periglaciar din România. Thesis raport, Babes-Bolyai University, Cluj-Napoca 2005.
- [17]Messerli B: Die eiszeitliche und die gegenwärtige Vergletscherung im Mittelmeerraum. Geogr Helv 1967, 22:105-228.
- [18]Schönswetter P, Stehlik I, Holderegger R, Tribsch A: Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 2005, 14(11):3547-3555.
- [19]Dzialuk A, Muchewicz E, Boratyński A, Montserrat JM, Boratyńska K, Burczyk J: Genetic variation of Pinus uncinata (Pinaceae) in the Pyrenees determined with cpSSR markers. Plant Syst Evol 2009, 277(3–4):197-205.
- [20]Vargas P, Rosselló JA, Oyama R, Güemes J: Molecular evidence for naturalness of genera in the tribe Antirrhineae (Scrophulariaceae) and three independent evolutionary lineages from the New World and the Old. Plant Syst Evol 2004, 249(3–4):151-172.
- [21]Jiménez JF, Sánchez-Gómez P, Güemes J, Rosselló JA: Phylogeny of snapdragon species (Antirrhinum; Scrophulariaceae) using non-coding cpDNA sequences. Isr J Plant Sci 2005, 53(1):47-54.
- [22]Vargas P, Carrió E, Guzmán B, Amat E, Güemes J: A geographical pattern of Antirrhinum (Scrophulariaceae) speciation since the Pliocene based on plastid and nuclear DNA polymorphisms. J Biogeogr 2009, 36(7):1297-1312.
- [23]Carrió E, Forrest AD, Güemes J, Vargas P: Evaluating species nonmonophyly as a trait affecting genetic diversity: A case study of three endangered species of Antirrhinum L. (Scrophulariaceae). Plant Syst Evol 2010, 288(1):43-58.
- [24]Wilson Y, Hudson A: The evolutionary history of Antirrhinum suggests that ancestral phenotype combinations survived repeated hybridizations. Plant J 2011, 66(6):1032-1043.
- [25]Andalo C, Cruzan MB, Cazettes C, Pujol B, Burrus M, Thébaud C: Post-pollination barriers do not explain the persistence of two distinct Antirrhinum subspecies with parapatric distribution. Plant Syst Evol 2010, 286(3):223-234.
- [26]Khimoun A, Cornuault J, Burrus M, Pujol B, Thébaud C, Andalo C: Ecology predicts parapatric distributions in two closely related Antirrhinum majus subspecies. Evol Ecol 2013, 27(1):51-64.
- [27]Tastard E, Ferdy JB, Burrus M, Thébaud C, Andalo C: Patterns of floral colour neighbourhood and their effects on female reproductive success in an Antirrhinum hybrid zone. J Evol Biol 2012, 25(2):388-399.
- [28]Rambaut A, Drummond AJ: Tracer 1.5.0. 2007. Available at: http://beast.bio.ed.ac.uk/Tracer webcite
- [29]Rogers AR, Harpending H: Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 1992, 9(3):552-569.
- [30]Alarcón M, Vargas P, Sáez L, Molero J, Aldasoro JJ: Genetic diversity of mountain plants: Two migration episodes of Mediterranean Erodium (Geraniaceae). Mol Phylogenet Evol 2012, 63(3):866-876.
- [31]Zhang LB, Comes HP, Kadereit JW: The temporal course of Quaternary diversification in the European high mountain endemic Primula sect. Auricula (Primulaceae). Int J Plant Sci 2004, 165(1):191-207.
- [32]Güemes J: Antirrhinum L. In Flora Iberica. vol. 13 edition. Edited by Castroviejo S, Herrero A, Benedí C, Rico E, Güemes J. Madrid: CSIC; 2009.
- [33]Sutton DA: A revision of the tribe Antirrhineae. Oxford: Oxford University Press; 1988.
- [34]Walsh H, Kidd M, Moum T, Friesen V: Polytomies and the power of phylogenetic inference. Evolution 1999, 53:932-937.
- [35]Magri D, Vendramin GG, Comps B, Dupanloup I, Geburek T, Gömöry D, Latałowa M, Litt T, Paule L, Roure JM, Tantau I, Van Der Knaap WO, Petit RJ, De Beaulieu JL: A new scenario for the quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytol 2006, 171(1):199-221.
- [36]Albre J, Gers C, Legal L: Molecular phylogeny of the Erebia tyndarus (Lepidoptera, Rhopalocera, Nymphalidae, Satyrinae) species group combining CoxII and ND5 mitochondrial genes: a case study of a recent radiation. Mol Phylogenet Evol 2008, 47(1):196-210.
- [37]Kropf M, Kadereit JW, Comes HP: Differential cycles of range contraction and expansion in European high mountain plants during the late quaternary: insights from Pritzelago alpina (L.) O. Kuntze (Brassicaceae). Mol Ecol 2003, 12(4):931-949.
- [38]Sánchez de Dios R, Benito-Garzón M, Sainz-Ollero H: Hybrid zones between two European oaks: a plant community approach. Plant Ecol 2006, 187(1):109-125.
- [39]Rivas Martinez S: Memoria Del Mapa De Series De Vegetaci6n De Espafia 1: 400000. Madrid: ICONA; 1987.
- [40]Vigo J, Ninot J: Los Pirineos. In La Vegetación de España. Edited by Peinado Lorea M, Rivas Martinez S. Alcalá de Henares: Col. Aula Abierta. Publ. Univ; 1987:351-384.
- [41]Dubreuil M, Riba M, Mayol M: Genetic structure and diversity in Ramonda myconi (Gesneriaceae): effects of historical climate change on a preglacial relict species. Am J Bot 2008, 95(5):577-587.
- [42]Jalut G, Amat AE, Riera I, Mora S, Fontugne M, Mook R, Bonnet L, Gauquelin T: Holocene climatic changes in the western mediterranean: installation of the mediterranean climate. C R Acad Sci II Sci Terre Planetes 1997, 325(5):327-334.
- [43]Valero-Garcés BL, González-Sampériz P, Delgado-Huertas A, Navas A, Machín J, Kelts K: Lateglacial and Late Holocene environmental and vegetational change in Salada Mediana, central Ebro Basin, Spain. Quat Int 2000, 73–74:29-46.
- [44]Gómez A, Lunt DH: Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula. In Phylogeography of Southern European Refugia. Edited by Weiss S, Ferrand N. NL: Dordrecht, Springer; 2007:155-188.
- [45]Villar L, Sesé JA, Ferrández JV: Atlas de la flora del Pirineo Aragonés. II. (Pyrolaceae-Orchidaceae. Síntesis). Huesca, Spain: Consejo de Protección de la Naturaleza de Aragón & Instituto de Estudios Altoaragonenses; 1997.
- [46]Segarra-Moragues JG, Palop-Esteban M, González-Candelas F, Catalán P: Nunatak survival vs. tabula rasa in the Central Pyrenees: a study on the endemic plant species Borderea pyrenaica (Dioscoreaceae). J Biogeogr 2007, 34(11):1893-1906.
- [47]Pèrez-Obiol R, Julià R: Climatic change on the iberian peninsula recorded in a 30,000-yr pollen record from lake banyoles. Quat Res 1994, 41(1):91-98.
- [48]Salvador L, Alía R, Agúndez D, Gil L: Genetic variation and migration pathways of maritime pine (Pinus pinaster Ait) in the Iberian peninsula. Theor Appl Genet 2000, 100(1):89-95.
- [49]Lumaret R, Mir C, Michaud H, Raynal V: Phylogeographical variation of chloroplast DNA in holm oak (Quercus ilex L.). Mol Ecol 2002, 11(11):2327-2336.
- [50]Sánchez Goñi M, Cacho I, Turon J, Guiot J, Sierro F, Peypouquet J, Grimalt J, Shackleton N: Synchroneity between marine and terrestrial responses to millennial scale climatic variability during the last glacial period in the Mediterranean region. Clim Dyn 2002, 19(1):95-105.
- [51]Moreno A, Cacho I, Canals M, Grimalt JO, Sánchez-Goñi MF, Shackleton N, Sierro FJ: Links between marine and atmospheric processes oscillating on a millennial time-scale. A multi-proxy study of the last 50,000 yr from the Alboran Sea (Western Mediterranean Sea). Quat Sci Rev 2005, 24(14–15):1623-1636.
- [52]García-Ramos G, Kirkpatrick M: Genetic models of adaptation and gene flow in peripheral populations. Evolution 1997, 51(1):21-28.
- [53]Cassel-Lundhagen A, Tammaru T, Windig JJ, Ryrholm N, Nylin S: Are peripheral populations special? Congruent patterns in two butterfly species. Ecography 2009, 32(4):591-600.
- [54]Lesica P, Allendorf FW: When are peripheral populations valuable for conservation? Conserv Biol 1995, 9(4):753-760.
- [55]Losos JB, Glor RE: Phylogenetic comparative methods and the geography of speciation. Trends Ecol Evol 2003, 18(5):220-227.
- [56]Petit RJ, Brewer S, Bordács S, Burg K, Cheddadi R, Coart E, Cottrell J, Csaikl UM, van Dam B, Deans JD: Identification of refugia and post-glacial colonisation routes of European white oaks based on chloroplast DNA and fossil pollen evidence. For Ecol Manag 2002, 156(1):49-74.
- [57]Schmitt T: Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Front Zool 2007, 4(11):1-13.
- [58]Templeton AR: Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 1998, 7(4):381-397.
- [59]Ronikier M, Schneeweiss GM, Schönswetter P: The extreme disjunction between Beringia and Europe in Ranunculus glacialis s. l. (Ranunculaceae) does not coincide with the deepest genetic split - a story of the importance of temperate mountain ranges in arctic-alpine phylogeography. Mol Ecol 2012, 21(22):5561-5578.
- [60]Albach DC, Schönswetter P, Tribsch A: Comparative phylogeography of the Veronica alpina complex in Europe and North America. Mol Ecol 2006, 15(11):3269-3286.
- [61]Schönswetter P, Tribsch A, Barfuss M, Niklfeld H: Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium Sternb. & Hoppe (Campanulaceae) in the European Alps. Mol Ecol 2002, 11(12):2637-2647.
- [62]Kerner A: Die natürlichen Floren im Gelände der deutschen Alpen. Die Dtsch Alpen für Einheimische und Fremde Geschildert 1871, 1:126-189.
- [63]Aeschimann D, Rasolofo N, Theurillat JP: Analysis of the flora of the Alps. 1: historical account and biodiversity. Analyse de la flore des Alpes 1: Historique et biodiversité 2011, 66(1):27-55.
- [64]Pampanini R: Essai Sur La Géographie Botanique Des Alpes Et En Particulier Des Alpes Sud-Orientales. Imprimerie Fragnière frères 1903.
- [65]Theissinger K, Bálint M, Feldheim KA, Haase P, Johannesen J, Laube I, Pauls SU: Glacial survival and post-glacial recolonization of an arctic-alpine freshwater insect (Arcynopteryx dichroa, Plecoptera, Perlodidae) in Europe. J Biogeogr 2013, 40(2):236-248.
- [66]Schmitt T, Hewitt GM: Molecular biogeography of the arctic-alpine disjunct burnet moth species Zygaena exulans (Zygaenidae, Lepidoptera) in the Pyrenees and Alps. J Biogeogr 2004, 31(6):885-893.
- [67]Petit RJ, Kremer A, Wagner DB: Finite island model for organelle and nuclear genes in plants. Heredity 1993, 71(6):630-641.
- [68]Ennos R, Sinclair W, Hu X, Langdon A: Using organelle markers to elucidate the history, ecology and evolution of plant populations. Systematics association special volume 1999, 57:1-19.
- [69]Soltis DE, Gitzendanner MA, Strenge DD, Soltis PS: Chloroplast DNA intraspecific phylogeography of plants from the Pacific Northwest of North America. Plant Syst Evol 1997, 206(1):353-373.
- [70]Hansen AK, Escobar LK, Gilbert LE, Jansen RK: Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. Am J Bot 2007, 94(1):42-46.
- [71]Azhagiri AK, Maliga P: Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants. Plant J 2007, 52(5):817-823.
- [72]Drummond A, Ashton B, Buxton S, Cheung M, Cooper A, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S: Geneious v5. 1. 2010. http://www.geneious.com webcite
- [73]Katoh K, Misawa K, Kuma KI, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30(14):3059-3066.
- [74]Ronquist F, Huelsenbeck JP: MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19(12):1572-1574.
- [75]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52(5):696-704.
- [76]Goloboff PA, Farris JS, Nixon KC: TNT, a free program for phylogenetic analysis. Cladistics 2008, 24(5):774-786.
- [77]Drummond AJ, Rambaut A: BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7(1):214.
- [78]Fernández-Mazuecos M, Vargas P: Congruence between distribution modelling and phylogeographical analyses reveals Quaternary survival of a toadflax species (Linaria elegans) in oceanic climate areas of a mountain ring range. New Phytol 2013, 198:1274-1289.
- [79]Bell CD, Soltis DE, Soltis PS: The age and diversification of the angiosperms re-revisited. Am J Bot 2010, 97(8):1296-1303.
- [80]Fernández-Mazuecos M, Vargas P: Historical isolation versus recent long-distance connections between Europe and Africa in bifid toadflaxes (Linaria sect. Versicolores). PLoS One 2011, 6(7):e22234.
- [81]Lemey P, Rambaut A, Drummond AJ, Suchard MA: Bayesian phylogeography finds its roots. PLoS Comput Biol 2009, 5(9):e1000520.
- [82]Yu Y, Harris A, He X: Rasp (Reconstruct Ancestral State In Phylogenies) 2.0 Beta. 2011. http://mnh.scu.edu.cn/soft/blog/RASP webcite
- [83]Ree RH, Smith SA: Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Syst Biol 2008, 57(1):4-14.
- [84]Clement M, Posada D, Crandall KA: TCS: a computer program to estimate gene genealogies. Mol Ecol 2000, 9(10):1657-1659.
- [85]Kelchner SA: The evolution of non-coding chloroplast DNA and its application in plant systematics. Ann Mo Bot Gard 2000, 87(4):482-498.
- [86]Souquet P, Bilotte M, Canerot J, Debroas E, Peybernés B, Rey J: Nouvelle interprétation de la structure des Pyrénées. C R Acad Sci Paris 1975, 281:609-612.
- [87]Souquet P, Mediavilla F: Nouvelle hypothèse sur la formation des Pyrénées. CR Acad Sci 1976, 282:2139-2142.
- [88]Rivas Martínez S, Báscones Carretero JC, Díaz González TE, Fernández González F, Loidi Arregui J: Vegetación del Pirineo occidental y Navarra: VI Excursión Internacional de Fitosociología (AEFA). Itinera Geobotanica 1991, 5:5-456.
- [89]Montserrat P: L’exploration floristique des Pyrénées occidentales. (The floristic exploration of West Pyrenees). Bol Soc Brot 1974, 47:227-241.
- [90]Villar L: La vegetación del Pirineo occidental: estudio de Geobotánica Ecológica. Príncipe de Viana Suplemento de Ciencias 1982, 263-434.
- [91]Izard M: Le Climat. In La Végétation des Pyrénees. Edited by Dupias G. Paris: Editions du CNRS; 1985:17-36.
- [92]Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25(11):1451-1452.
- [93]Excoffier L, Smouse PE, Quattro JM: Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 1992, 131(2):479-491.
- [94]Excoffier L, Laval G, Schneider S: Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinformatics Online 2005, 1:47.
- [95]Corander J, Marttinen P, Sirén J, Tang J: Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC bioinformatics 2008, 9:539.
- [96]Corander J, Tang J: Bayesian analysis of population structure based on linked molecular information. Math Biosci 2007, 205(1):19-31.
- [97]Dupanloup I, Schneider S, Excoffier L: A simulated annealing approach to define the genetic structure of populations. Mol Ecol 2002, 11(12):2571-2581.
- [98]Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 1989, 123(3):585-595.
- [99]Fu YX: Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 1997, 147(2):915-925.
- [100]Slatkin M, Hudson RR: Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 1991, 129(2):555-562.
- [101]Harpending HC: Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 1994, 66(4):591-600.
- [102]Excoffier L, Lischer HEL: Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 2010, 10(3):564-567.