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Quaternary radiation of bifid toadflaxes (Linaria sect. Versicolores) in the Iberian Peninsula: low taxonomic signal but high geographic structure of plastid DNA lineages

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Abstract

Phylogeographic analysis provides insights into the micro-evolutionary mechanisms driving recent radiations. Here we conducted a phylogeographic analysis of the Iberian clade of Linaria subsect. Versicolores. This lineage includes eight species and subspecies endemic or subendemic to the Iberian Peninsula that diversified in the Quaternary. We obtained 159 sequences of three plastid DNA regions from 53 individuals of the study group representing all recognized taxa. Phylogenetic, haplotype network, dating and population genetic analyses were conducted. In addition, the radiation hypothesis (common ancestry and rapid speciation) was tested. The results revealed two major clades that diverged in the Pleistocene. Low taxonomic signal of plastid DNA sequences was found as a result of rapid diversification. Indeed, the study group is herein described as an evolutionary radiation because of its common ancestry and diversification rates in line with those of other recent plant radiations. Interestingly, a high geographic structure of plastid DNA lineages was revealed, with a major genetic discontinuity separating south-eastern populations from those of the rest of Iberia. Based on dating results, we rule out a marine barrier as the cause behind this discontinuity, and hypothesize a role of edaphic specialization in differentiation of the two major clades. These results provide relevant information on the evolutionary dynamics of recent plant radiations in the western Mediterranean hotspot.

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References

  • Albaladejo RG, Fuertes Aguilar J, Aparicio A, Nieto Feliner G (2005) Contrasting nuclear-plastidial phylogenetic patterns in the recently diverged Iberian Phlomis crinita and P. lychnitis lineages (Lamiaceae). Taxon 54:987–998

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Balao F, Valente LM, Vargas P, Herrera J, Talavera S (2010) Radiative evolution of polyploid races of the Iberian carnation Dianthus broteri (Caryophyllaceae). New Phytol 187:542–551

    Article  CAS  PubMed  Google Scholar 

  • Bittkau C, Comes HP (2009) Molecular inference of a late Pleistocene diversification shift in Nigella s. lat. (Ranunculaceae) resulting from increased speciation in the Aegean archipelago. J Biogeogr 36:1346–1360

    Article  Google Scholar 

  • Blanco-Pastor JL, Vargas P (2013) Autecological traits determined two evolutionary strategies in Mediterranean plants during the Quaternary: low differentiation and range expansion versus geographical speciation in Linaria. Molec Ecol 22:5651–5668

    Article  CAS  Google Scholar 

  • Blanco-Pastor JL, Vargas P, Pfeil BE (2012) Coalescent simulations reveal hybridization and incomplete lineage sorting in Mediterranean Linaria. PLoS One 7:e39089

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659

    Article  CAS  Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Amer J Bot 75:1443–1458

    Article  Google Scholar 

  • Cummings MP, Neel MC, Shaw KL (2008) A genealogical approach to quantifying lineage divergence. Evolution 62:2411–2422

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772–772

    Article  CAS  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:699–710

    Article  CAS  Google Scholar 

  • Drummond AJ, Ashton B, Cheung M, Heled J, Kearse M, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious version 5.0. Available at http://www.geneious.com.

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molec Biol Evol 29:1969–1973

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Emberger L (1930) Materiaux pour l’étude de la flore et de la végétation du Maroc. Fascicule 1. Bull Soc Hist Nat Afrique N 21:101–114

    Google Scholar 

  • Escudero M, Valcárcel V, Vargas P, Luceño M (2008) Evolution in Carex L. sect. Spirostachyae (Cyperaceae): a molecular and cytogenetic approach. Org Divers Evol 7:271–291

    Article  Google Scholar 

  • Felsenstein J (2005) PHYLIP (Phylogeny Inference Package) version 3.6. Department of Genome Sciences, University of Washington, Seattle. Available at http://evolution.genetics.washington.edu/phylip.html.

  • Fernández-Mazuecos M, Vargas P (2010) Ecological rather than geographical isolation dominates Quaternary formation of Mediterranean Cistus species. Molec Ecol 19:1381–1395

    Article  Google Scholar 

  • Fernández-Mazuecos M, Vargas P (2011) Historical isolation versus recent long-distance connections between Europe and Africa in bifid toadflaxes (Linaria sect. Versicolores). PLoS One 6:e22234

    Article  PubMed Central  PubMed  Google Scholar 

  • Fernández-Mazuecos M, Vargas P (2013) 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 198:1274–1289

    Article  PubMed  Google Scholar 

  • Fernández-Mazuecos M, Blanco-Pastor JL, Gómez JM, Vargas P (2013a) Corolla morphology influences diversification rates in bifid toadflaxes (Linaria sect. Versicolores). Ann Bot (Oxford) 112:1705–1722

    Article  Google Scholar 

  • Fernández-Mazuecos M, Blanco-Pastor JL, Vargas P (2013b) A phylogeny of toadflaxes (Linaria Mill.) based on nuclear internal transcribed spacer sequences: systematic and evolutionary consequences. Int J Pl Sci 174:234–249

    Article  Google Scholar 

  • Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253:769–778

    Article  PubMed  Google Scholar 

  • Guzmán B, Lledó MD, Vargas P (2009) Adaptive radiation in Mediterranean Cistus (Cistaceae). PLoS One 4:e6362

    Article  PubMed Central  PubMed  Google Scholar 

  • Hamilton MB (1999) Four primer pairs for the amplification of chloroplast intergenic regions with intraspecific variation. Molec Ecol 8:521–523

    CAS  Google Scholar 

  • Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W (2008) GEIGER: investigating evolutionary radiations. Bioinformatics 24:129–131

    Article  CAS  PubMed  Google Scholar 

  • Hewitt GM (1988) Hybrid zones–natural laboratories for evolutionary studies. Trends Ecol Evol 3:158–167

    Article  CAS  PubMed  Google Scholar 

  • Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hughes C, Eastwood R (2006) Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc Natl Acad Sci USA 103:10334–10339

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255

    Article  PubMed  Google Scholar 

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Syst Biol 56:887–895

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Magallón S, Sanderson MJ (2001) Absolute diversification rates in angiosperm clades. Evolution 55:1762–1780

    Article  PubMed  Google Scholar 

  • Maire R (1941) Contributions à l’étude de la flore de L’Afrique du Nord. Fascicule 30. Bull Soc Hist Nat Afrique N 31:99–114

    Google Scholar 

  • Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190

    Article  PubMed  Google Scholar 

  • Médail F, Quézel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean basin. Ann Missouri Bot Gard 84:112–127

    Article  Google Scholar 

  • Meléndez Hevia I (2004) Geología de España: una historia de seiscientos millones de años. Ediciones Rueda, Alcorcón

    Google Scholar 

  • Monmonier MS (1973) Maximum difference barriers: an alternative numerical regionalization method. Geogr Anal 5:245–261

    Article  Google Scholar 

  • Mutke J, Sommer JH, Kreft H, Kier G, Barthlott W (2011) Vascular plant diversity in a changing world: global centres and biome-specific patterns. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, Berlin, pp 83–96

    Chapter  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Olmstead RG, Reeves PA (1995) Evidence for the polyphyly of the Scrophulariaceae based on chloroplast rbcL and ndhF sequences. Ann Missouri Bot Gard 82:176–193

    Article  Google Scholar 

  • Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481

    Article  Google Scholar 

  • Ortiz MÁ, Tremetsberger K, Stuessy TF, Terrab A, García-Castaño JL, Talavera S (2009) Phylogeographic patterns in Hypochaeris section Hypochaeris (Asteraceae, Lactuceae) of the western Mediterranean. J Biogeogr 36:1384–1397

    Article  Google Scholar 

  • Pérez-García FJ, Medina-Cazorla JM, Martínez-Hernández F, Garrido-Becerra JA, Mendoza-Fernández AJ, Salmerón-Sánchez E, Mota JF (2012) Iberian Baetic endemic flora and the implications for a conservation policy. Ann Bot Fennici 49:43–54

    Article  Google Scholar 

  • Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300:1563–1565

    Article  CAS  PubMed  Google Scholar 

  • Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molec Ecol 14:689–701

    Article  CAS  Google Scholar 

  • Rajakaruna N (2004) The edaphic factor in the origin of plant species. Int Geol Rev 46:471–478

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer version 1.4. Available at http://beast.bio.ed.ac.uk/Tracer.

  • Rodríguez-Sánchez F, Pérez-Barrales R, Ojeda F, Vargas P, Arroyo J (2008) The Strait of Gibraltar as a melting pot for plant biodiversity. Quaternary Sci Rev 27:2100–2117

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed Central  PubMed  Google Scholar 

  • Sáez L, Bernal M (2009) Linaria Mill. In: Castroviejo S, Herrero A, Benedí C, Rico E, Güemes J (eds) Flora iberica, vol 13. CSIC, Madrid, pp 232–324

    Google Scholar 

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Amer J Bot 94:275–288

    Article  CAS  Google Scholar 

  • Sturmbauer C, Husemann M, Danley PD (2011) Explosive speciation and adaptive radiation of East African cichlid fishes. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, Berlin, pp 333–362

    Chapter  Google Scholar 

  • Suc JP (1984) Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307:429–432

    Article  Google Scholar 

  • Sutton DA (1988) A revision of the tribe Antirrhineae. Oxford University Press, Oxford

    Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633

    CAS  Google Scholar 

  • Terrab A, Talavera S, Arista M, Paun O, Stuessy TF, Tremetsberger K (2007) Genetic diversity at chloroplast microsatellites (cpSSRs) and geographic structure in endangered West Mediterranean firs (Abies spp., Pinaceae). Taxon 56:409–416

    Google Scholar 

  • Tsitrone A, Kirkpatrick M, Levin DA (2003) A model for chloroplast capture. Evolution 57:1776–1782

    Article  PubMed  Google Scholar 

  • Valdés B (1970) Taxonomía experimental del género Linaria V. Hibridación interespecífica. Acta Phytotax Barcinon 4:1–24

    Google Scholar 

  • Valente LM, Savolainen V, Vargas P (2010) Unparalleled rates of species diversification in Europe. Proc Roy Soc London B Biol Sci 277:1489–1496

    Article  Google Scholar 

  • Vargas P, Carrió E, Guzmán B, Amat E, Güemes J (2009) A geographical pattern of Antirrhinum (Scrophulariaceae) speciation since the Pliocene based on plastid and nuclear DNA polymorphisms. J Biogeogr 36:1297–1312

    Article  Google Scholar 

  • Vargas P, Valente LM, Blanco-Pastor JL, Liberal I, Guzmán B, Cano E, Forrest A, Fernández-Mazuecos M (2014) Testing the biogeographical congruence of palaeofloras using molecular phylogenetics: snapdragons and the Madrean-Tethyan flora. J Biogeogr 41:932–943

    Article  Google Scholar 

  • Viano J (1973) Resultats caryologiques de quelques especes de Linaria et Chaenorrhinum recoltees au sud de la Peninsule Iberique. Bol Soc Brot Supl 47:323–331

    Google Scholar 

  • Viano J (1978a) Croisements experimentaux interspecifiques au sein du genre Linaria. Caryologia 31:383–425

    Article  Google Scholar 

  • Viano J (1978b) Les linaires à graines aptères du bassin méditerranéen occidental. 1. Linaria sect. Versicolores. Candollea 33:33–88

    Google Scholar 

  • Willyard A, Cronn R, Liston A (2009) Reticulate evolution and incomplete lineage sorting among the ponderosa pines. Molec Phylogenet Evol 52:498–511

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Emilio Cano for laboratory assistance; Llorenç Sáez for providing plant material of L. viscosa subsp. crassifolia; Enrique Sánchez-Gullón, Belén Estébanez, Nagore G. Medina, José Luis Blanco-Pastor, Joaquín Ramírez, Enrique Rico, Francisco Valtueña, Isabel Marques and the MA, RNG and UPOS herbaria for additional plant materials or localities; José Luis Blanco-Pastor and Isabel Liberal for comments that improved the quality of the manuscript. This work was supported by the Spanish Ministry of Science and Innovation through project CGL2009-10031 and by the Spanish Ministry of Education through a FPU fellowship (AP2007-01841) to M.F.-M.

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Correspondence to Mario Fernández-Mazuecos.

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606_2014_1161_MOESM1_ESM.pdf

Supplementary material 1 (PDF 19 kb) Online Resource 1. GenBank accession numbers of plastid DNA sequences of the Iberian clade of Linaria subsect. Versicolores. Individuals are coded as in Table 1 and Fig. 1

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Fernández-Mazuecos, M., Vargas, P. Quaternary radiation of bifid toadflaxes (Linaria sect. Versicolores) in the Iberian Peninsula: low taxonomic signal but high geographic structure of plastid DNA lineages. Plant Syst Evol 301, 1411–1423 (2015). https://doi.org/10.1007/s00606-014-1161-2

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