Skip to main content
SpringerLink
Log in

Molecular confirmation of the hybrid origin of the critically endangered western Mediterranean endemic Sonchus pustulatus (Asteraceae: Sonchinae)

  • Regular Paper
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The critically endangered composite Sonchus pustulatus Willk. despite being known from fewer than ten locations in southern Spain and northern Africa, has never been characterized in robust phylogenetic context. Here, we report molecular evidence that strongly supports a hybrid origin for S. pustulatus. Although parentage cannot be identified with certainty, analysis of DNA sequence variation from the internal transcribed spacer (ITS) region of nuclear ribosomal DNA (nrDNA) supports a phylogenetic placement of S. pustulatus close to other species in the poorly known section Pustulati, whereas examination of chloroplast DNA (cpDNA) places S. pustulatus most closely with species from the sections Sonchus and Asperi. This is one of several instances of topological non-concordance reported for the genus Sonchus. Monophyly of S. pustulatus in both gene genealogies supports the null hypothesis of a single origin, and the relatively large amount of nucleotide substitutions is indicative of an origin in the range of millions of years. A hypothesis of a northern African origin of S. pustulatus followed by dispersal to the Iberian Peninsula during the Messinian salinity crisis/later Quaternary glaciations is proposed on the basis of biogeographic patterns and calibrated estimations of molecular evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Albadalejo 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 54:987–997

    Google Scholar 

  • Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, Oxford, 215 pp

  • Arnold MA, Bouck AC, Cornman RS (2003) Verne Grant and Louisiana irises: is there anything new under the sun? New Phytol 161:143–149

    Article  Google Scholar 

  • Baldwin BG, Sanderson MJ (1998) Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc Natl Acad Sci U S A 95:9402–9406

    Article  PubMed  CAS  Google Scholar 

  • Bañares Á, Blanca G, Gümes J, Moreno JC, Oritz S (eds) (2004) Atlas y Libro Rojo de la Flora Vascular Amenazada de Espana: Taxones Prioritarios. Dirección General de Conservación de la Naturaleza. Madrid, Spain, 1072 pp

  • Barrón E, Peyrot D (2006) La vegetación forestal en el Terciario. In: Carrión JS, Fernández S, Fuentes N (eds) Paleoambientes y cambio climático. Fundación Séneca—Agencia de Ciencia y Tecnología de la Región de Murcia, Murcia, Spain, pp 56–76

    Google Scholar 

  • Boulos L (1972) Révision systématique du genre Sonchus L. s.l. I. Introduction et classification. Bot Not 125:287–305

    Google Scholar 

  • Boulos L (1973) Révision systématique du genre Sonchus L. s.l. IV. Sous-genre 1. Sonchus. Bot Not 126:155–196

    Google Scholar 

  • Bremer K (1988) The limits of amino acid sequence data in angiosperm phylogenetic reconstruction. Evolution 42:795–803

    Article  CAS  Google Scholar 

  • Cheddadi R, De Beaulieu J-L, Jouzel J, Andrieu-Ponel V, Laurent J-M, Reille M, Raynaud MD, Bar-Hen A (2005) Similarity of vegetation dynamics during interglacial periods. Proc Natl Acad Sci U S A 102:13939–13943

    Article  PubMed  CAS  Google Scholar 

  • Collina-Girard J (2001) L’Atlantide devant le détroit de Gibraltar? Mythe et géologie. Earth Planet Sci 333:233–240

    Google Scholar 

  • Comes HP, Abbott RJ (2001) Molecular phylogeography, reticulation, and lineage sorting in Mediterranean Senecio sect. Senecio (Asteraceae). Evolution 55:1943–1962

    PubMed  CAS  Google Scholar 

  • De Jong H (1998) In search of historical biogeographic patterns in the western Mediterranean terrestrial fauna. Biol J Linn Soc 65:99–164

    Article  Google Scholar 

  • Doyle JJ, Doyle JL, Rauscher JT, Brown AHD (2004) Diploid and polyploid reticulate evolution throughout the history of the perennial soybeans (Glycine subgenus Glycine). New Phytol 161:121–132

    Article  CAS  Google Scholar 

  • Ellstrand NC, Whittikus R, Rieseberg LH (1996) Distribution of spontaneous plant hybrids. Proc Natl Acad Sci U S A 93:5090–5093

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fennane M, Ibn Tattou M (1998) Catalogue des plantes vascularies rares, menacées ou endémiques du Maroc. Bocconea 8:5–243

    Google Scholar 

  • Fuertes Aguilar J, Nieto Feliner G (2003) Additive polymorphisms and reticulation in an ITS phylogeny of thrifts (Armeria, Plumbaginaceae). Mol Phylogenet Evol 28:430–447

    Article  PubMed  CAS  Google Scholar 

  • Goldman N (1993) Statistical tests of models of DNA substitution. J Mol Evol 36:182–198

    Article  PubMed  CAS  Google Scholar 

  • Grant V (1981) Plant speciation, 2nd edn. Columbia University Press, New York, 563 pp

  • Gutiérrez Larena B, Fuertes Aguilar J, Nieto Feliner G (2002) Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Mol Ecol 11:1965–1974

    Article  PubMed  Google Scholar 

  • Hegarty MJ, Hiscock SJ (2005) Hybrid speciation in plants: new insights from molecular studies. New Phytol 165:411–423

    Article  PubMed  CAS  Google Scholar 

  • Jobst J, King K, Hemleben V (1998) Molecular evolution of the internal transcribed spacers (ITS1 and ITS2) and phylogenetic relationships among species of the family Cucurbitaceae. Mol Phylogenet Evol 9:204–219

    Article  PubMed  CAS  Google Scholar 

  • Kim S-C, Crawford DJ, Jansen RK (1996a) Phylogenetic relationships among the genera of the subtribe Sonchinae (Asteraceae): evidence from ITS sequences. Syst Bot 21:417–432

    Article  Google Scholar 

  • Kim S-C, Crawford DJ, Francisco-Ortega J, Santos-Guerra A (1996b) A common origin for woody Sonchus and five related genera in the Macaronesian Islands: molecular evidence for extensive radiation. Proc Natl Acad Sci U S A 93:7743–7748

    Article  PubMed  CAS  Google Scholar 

  • Kim S-C, Lu CT, Lepschi BJ (2004) Phylogenetic positions of Actites megalocarpa and Sonchus hydrophilus (Sonchinae: Asteraceae) based on ITS and chloroplast non-coding DNA sequences. Aust Syst Bot 17:73–81

    Article  CAS  Google Scholar 

  • Kim S-C, Lee C, Mejías JA (2007) Phylogenetic analysis of chloroplast DNA matK gene and ITS of nrDNA sequences reveals polyphyly of the genus Sonchus and new relationships among the subtribe Sonchinae (Asteraceae: Cichorieae). Mol Phylogenet Evol 44:578–597

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1980) Simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Knobloch IW (1972) Intergeneric hybridization in flowering plants. Taxon 21:97–103

    Article  Google Scholar 

  • Lee C, Kim S-C, Lundy K, Santos-Guerra A (2005) Chloroplast DNA phylogeny of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian Islands. Am J Bot 92:2072–2085

    Article  CAS  Google Scholar 

  • Levin DA (2002) The role of chromosomal change in plant evolution. Oxford University Press, Oxford, 230 pp

  • Mallet J (2007) Hybrid speciation. Nature 446:279–283

    Article  PubMed  CAS  Google Scholar 

  • McBreen K, Lockhart PJ (2006) Reconstructing reticulate evolutionary histories of plants. Trends Plant Sci 11:398–404

    Article  PubMed  CAS  Google Scholar 

  • Mejías JA (1988) Diferencias cariológicas y morfológicas entre Sonchus pustulatus Willk. y Sonchus tenerrimus L. Lagascalia 15 [Suppl]:345–354

    Google Scholar 

  • Mejías JA, Andrés C (2004) Karyological studies in Iberian Sonchus (Asteraceae: Lactuceae): S. oleraceus, S. microcephalus and S. asper and a general discussion. Folia Geobot 39:275–291

    Article  Google Scholar 

  • Mota JF, Cueto M, Pérez-García FJ, Garrido JA, Martínez-Hernández F, Medina-Cazorla JM, Sola AJ, Schwarzer H (2005) Contribución al conocimiento de la flora de Andalucía: citas novedosas de la provincia de Almería, el elemento estenócoro. Acta Bot Malacitan 30:227–231

    Google Scholar 

  • Nieto Feliner G, Fuertes Aguilar J, Roselló JA (2002) Reticulation or divergence: the origin of a rare serpentine endemic assessed with chloroplast, nuclear and RAPD markers. Plant Syst Evol 231:19–38

    Article  Google Scholar 

  • Okuyama Y, Fujii N, Wakabayashi M, Kawakita A, Ito M, Watanabe M, Murakami N, Kato M (2005) Nonuniform concerted evolution and chloroplast capture: heterogeneity of observed introgression patterns in three molecular data partition phylogenies of Asian Mitella (Saxifragaceae). Mol Biol Evol 22:285–296

    Article  PubMed  CAS  Google Scholar 

  • Ortiz A, Tremetsberger K, Talavera S, Stuessy TF, García-Castaño JL (2007) Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes. Mol Ecol 16:541–552

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Crandall K (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Pou A (1988) La Erosión. Ministerio de Obras Públicas y Urbanismo. Madrid, 121 pp

  • Rieseberg LH (1991) Homoploid reticulate evolution in Helianthus (Asteraceae): evidence from ribosomal genes. Am J Bot 78:1218–1237

    Article  Google Scholar 

  • Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, Durphy JL, Schwarzbach AE, Donovan LA, Lexer C (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216

    Article  PubMed  CAS  Google Scholar 

  • Roux J, Boulos L (1972) Révision systématique du genre Sonchus L. s.l. II. Étude caryologique. Bot Not 125:306–309

    Google Scholar 

  • Saito N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Sang T, Crawford DJ, Kim S-C, Stuessy TF (1994) Radiation of the endemic genus Dendroseris (Asteraceae) on the Juan Fernandez Islands: evidence from sequences of the ITS regions of nuclear ribosomal DNA. Am J Bot 81:1494–1501

    Article  CAS  Google Scholar 

  • Soltis DE, Kuzoff RK (1995) Discordance between nuclear and chloroplast phylogenies in the Heuchera group (Saxifragaceae). Evolution 49:727–742

    Article  Google Scholar 

  • Soltis DE, Johnson LA, Looney C (1996) Discordance between ITS and chloroplast topologies in the Boykinia group (Saxigragaceae). Syst Bot 21:169–185

    Article  Google Scholar 

  • Stebbins GL, Jenkins JA, Walters MS (1953) Chromosomes and phylogeny in the Compositae, tribe Cichorieae. Univ Calif Publ Bot 26:401–430

    Google Scholar 

  • Swofford DL (2001) PAUP*: phylogenetic analysis using parsimony (*and other methods) version 4.0. Sinauer, Sunderland

    Google Scholar 

  • Talavera S, Devesa JA, Galiano EF (1984) Notas cariosistemáticas sobre plantas norteafricanas. I. Compositae. Candollea 39:271–280

    Google Scholar 

  • Thompson JD (2003) Plant evolution in the Mediterranean. Oxford University Press, Oxford, 293 pp

  • Veith M, Mayer C, Samraoui B, Barroso DD, Bogaerts S (2004) From Europe to Africa and vice versa: evidence for intercontinental dispersal in ribbed salamanders (Genus Pleurodeles). J Biogeogr 31:159–171

    Article  Google Scholar 

  • Wendel JF, Schnabel A, Seelanan T (1995) An unusual ribosomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. Mol Phylogenet Evol 4:298–313

    Article  PubMed  CAS  Google Scholar 

  • Whelan S, Goldman N (1999) Distributions of statistics used for the comparison of models of sequence evolution in phylogenetics. Mol Biol Evol 16:1292–1299

    CAS  Google Scholar 

  • Wojciechowski MF, Sanderson MJ, Fu FM (1999) Evidence on the monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA ITS and chloroplast DNA trnL intron data. Syst Bot 24:409–437

    Article  Google Scholar 

  • Yokoyama Y, Lambeck K, de Deckker P, Johnston P, Fifield LK (2000) Timing of the Last Glacial Maximum from observed sea-level minima. Nature 406:713–716

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This project was supported, in part, by an Academic Senate Grant, Regents’ Faculty Fellowship, and Agricultural Experiment Station funds from the University of California at Riverside, to S.-C. Kim. We are also grateful for financial support by the Spanish Ministerio de Educación y Ciencia (grant CGL 2006-00817) and Junta de Andalucía (Group RNM-210). Suggestions from two anonymous reviewers and the editor greatly improved the earlier version of the manuscript. We thank Li Yao for cloning S. pustulatus. Special thanks are due to Stephen Jury for information of the Sonchus species in Morocco.

Author information

Authors and Affiliations

  1. Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

    Seung-Chul Kim & Pesach Lubinsky

  2. Departmento de Biología Vegetal y Ecología, Universidad de Sevilla, Sevilla, Spain

    Jose A. Mejías

Authors
  1. Seung-Chul Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jose A. Mejías
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pesach Lubinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seung-Chul Kim.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10265_2008_166_MOESM1_ESM.pdf

Figure S1. Geographic locations of known (solid) and reported (gray) populations of Sonchus subgenus Sonchus section Pustulati taxa. Squares S. pustulatus, circles S. fragilis, triangles S. masguindalii, and stars S. briquetianus. Populations in gray have not been confirmed during the past 15 years. X indicate the peaks of mountains, followed by altitudes in meters. (PDF 131 kb)

10265_2008_166_MOESM2_ESM.doc

Appendix S1. Additional samples of species in section Pustulati used in this study, including the locality, voucher and herbarium numbers, and GenBank accession numbers. SEV Herbarium Universidad de Sevilla. RNG Herbarium of the University of Reading. Accession numbers with asterisks were reported previously in Kim et al. (2007) (DOC 48 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, SC., Mejías, J.A. & Lubinsky, P. Molecular confirmation of the hybrid origin of the critically endangered western Mediterranean endemic Sonchus pustulatus (Asteraceae: Sonchinae). J Plant Res 121, 357–364 (2008). https://doi.org/10.1007/s10265-008-0166-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-008-0166-8

Keywords

Search

Navigation