Nuclear ribosomal DNA and karyotypes indicate a NW African origin of South American Hypochaeris (Asteraceae, Cichorieae)

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Abstract

Hypochaeris has a disjunct distribution, with more than 15 species in the Mediterranean region, the Canary Islands, Europe, and Asia, and more than 40 species in South America. Previous studies have suggested that the New World taxa have evolved from ancestors similar to the central European H. maculata. Based on internal transcribed spacer (ITS) sequences and fluorescence in situ hybridization (FISH) with 5S and 18S–25S rDNA of the previously overlooked Hypochaeris angustifolia from Moyen Atlas, Morocco, we show that it is sister to the entire South American group. A biogeographic analysis supports the hypothesis of long-distance dispersal from NW Africa across the Atlantic Ocean for the origin of the South American taxa rather than migration from North America, through the Panamian land bridge, followed by subsequent extinction in North America. With the assumption of a molecular clock, the trans-Atlantic dispersal from NW Africa to South America is roughly estimated to have taken place during Pliocene or Pleistocene.

Introduction

The genus Hypochaeris (Asteraceae, Cichorieae) is distributed in North Africa, the Canary Islands, Europe, Asia, and South America. The co-occurrence with its sister genus Leontodon in the Mediterranean region (North Africa and S Europe) and the abundance of Old World species in this region suggest a Mediterranean origin of Hypochaeris (Samuel et al., 2003, Stebbins, 1971). The Hypochaeridinae are distributed in Eurasia and North Africa (Bremer, 1994). There are no other Hypochaeridinae in South America (Bremer, 1994). Old World Hypochaeris (c. 15 species) also contain greater karyotypic (chromosome numbers x = 3, 4, 5, and 6 and all symmetric karyotypes; Cerbah et al., 1998a, Cerbah et al., 1999; see Fig. 1, Fig. 2) and genetic diversity (Cerbah et al., 1998b, Samuel et al., 2003) than the South American group (c. 40 species; Samuel et al., 2003, Weiss-Schneeweiss et al., 2003). Old World Hypochaeris have been divided among four well defined sections on the basis of pappus characters (Hoffmann, 1893). This classification has been supported by chromosome numbers (Cerbah et al., 1998a) and DNA sequence data (Samuel et al., 2003). The sequence data suggest that Hoffmann’s (1893) fifth section Robertia does not belong within Hypochaeris, but rather within Leontodon (Cerbah et al., 1998b, Samuel et al., 2003). The monophyletic South American species (Samuel et al., 2003) all have asymmetrical, bimodal karyotypes with n = 4 (Weiss et al., 2003, Weiss-Schneeweiss et al., 2003), but differ from each other both morphologically and ecologically (e.g., Bortiri, 1999). They have been included within the otherwise Eurasian sect. Achyrophorus containing H. grandiflora, H. maculata, and H. uniflora based on the presence of just one row of pappus hairs (Hoffmann, 1893). The Eurasian sect. Achyrophorus has n = 5 and similar karyotypes, including also localization of rDNA loci (Cerbah, 1997; Weiss-Schneeweiss et al., unpubl.).

The biogeographic origin of the South American group is still problematic. Two conflicting hypotheses exist to explain how Hypochaeris arrived in South America given its absence from North America. (1) Stebbins’ (1971) hypothesis is based primarily on the assumption that the asymmetrical, bimodal karyotype is generally a derived genomic character in flowering plants. It is found in the South American group, in contrast to Old World Hypochaeris, which have rather symmetrical karyotypes. Stebbins (1971) suggested that Hypochaeris may have existed in North America during the Tertiary as small populations in pioneer habitats, a situation which might have favored evolution of asymmetrical, bimodal karyotypes (two large and two small chromosome pairs). After entering South America during the Pliocene, perhaps by migration through the Panamian land bridge, Hypochaeris might have diversified into different environments, and the North American populations gone extinct. (2) Samuel et al. (2003) suggested that there might be a simpler and hence more attractive explanation, namely long-distance dispersal directly to South America. DNA sequence evidence of Samuel et al. (2003) showed that two Old World sections (Achyrophorus and Metabasis) are closely related with the South American group. Based on karyotypic similarity of H. maculata and relatives of the Eurasian sect. Achyrophorus and the South American species (both possess two 18S–25S rDNA loci, and the intrachromosomal location of the single 5S rDNA locus is the same), Weiss-Schneeweiss et al. (2003) presented a model of chromosomal changes during evolution from a H. maculata-like ancestor, i.e., H. maculata or H. uniflora, which share similar karyotypes, or their unknown/extinct relative, to the South American species. These detailed karyotypic analyses, including particularly the number and localization of 5S and 45S rRNA genes by FISH, allowed the hypothesis that one species of this group (or a related ancestral taxon of sect. Achyrophorus) gave rise to the South American group, although sect. Achyrophorus differs from the South American group by its chromosome number (n = 5 vs. n = 4).

Determining the closest relative of the South American group could give a clue to migration or dispersal as an agent of evolution. Oberprieler and Vogt (2002) investigated the basic karyotype morphology of the previously poorly studied Moroccan endemic, Hypochaeris angustifolia (Litard & Maire) Maire, and showed it to have n = 4 with three pairs of chromosomes carrying satellites (rRNA genes). H. angustifolia also has a single row of pappus hairs like other members of sect. Achyrophorus (Galán de Mera and Vicente Orellana, 1998), but it has not yet been included in any phylogenetic analysis. The basic chromosome number and asymmetric karyotype of H. angustifolia suggest that this species could be a closer relative of the South American group than H. maculata.

We therefore extended the previous molecular phylogenetic study of Hypochaeris (Samuel et al., 2003) by including H. angustifolia and other missing taxa using a nuclear (ITS) and a chloroplast (rps16 intron) sequence. A detailed study of the karyotype of H. angustifolia was also carried out using FISH. The specific purposes of this study were to: (1) determine the relationship of H. angustifolia to other Old and New World taxa; and (2) interpret its relationships in context of the biogeographic origin (time and place) of the South American group.

Section snippets

Plant material

We sampled leaves of H. angustifolia and other Western Mediterranean species not previously included in a phylogenetic analysis (Samuel et al., 2003; H. arachnoidea, H. leontodontoides, H. rutea, and H. salzmanniana; Table 1) in the field. Because this study focuses on H. angustifolia, we sequenced five individuals in Morocco collected from throughout the geographical range of the species. Species classification of Moroccan and Spanish taxa follows Talavera, 1987, Oberprieler, 2002, and Galán

DNA sequences

PCR-amplified ITS fragments showed a single band when examined on agarose gels. The aligned ITS1 is 263 nucleotides (nt) long (length of individual sequences: 250–254 nt). The 5.8S rDNA gene is 164 nt long, has no gaps and few mutations (five sites in Hypochaeris plus four sites in outgroup taxa). The aligned ITS2 is 231 nt long (length of individual sequences: 202–226 nt). Length variation is mainly in the loop of helix 2A (see below). Eleven sites in all Hypochaeris sequences are polymorphic

Usefulness of ITS sequences for phylogenetic inference in Hypochaeris

A number of molecular genetic processes impact ITS sequences in ways that may mislead phylogenetic inference (Álvarez and Wendel, 2003). The main problem is the existence in many plant genomes of extensive sequence variation and presence of paralogous loci, which are derived from a duplication event (Álvarez and Wendel, 2003, Bailey et al., 2003). Hypochaeris species have one or two major 18S–5.8S–28S rDNA loci located in the nucleolar organizer regions of different chromosomes (Cerbah et al.,

Acknowledgments

We sincerely thank C.M. Baeza, S. Gómez, A. Jimenez and M.J. Parra (Concepción), E. Urtubey (La Plata), P. Schönswetter and A. Tribsch (Oslo), G.M.A. Fischer and R. Hössinger (Wien), D. Dimitrova (Sofija), M. Weigend (Berlin), E. Beltrán (San Cristóbal de La Laguna), E. Rico and J. Sánchez (Salamanca) for collection of plant material, M. Barfuss (Wien) for internal primer design, G. Schneeweiss (Wien) for introduction to r8s, and two anonymous reviewers for helpful comments on a previous

References (77)

  • N. Barghi et al.

    Karyological studies in some Hypochoeris spp. (Compositae) from Sicily

    Plant Syst. Evol.

    (1989)
  • Bortiri, E., 1999. Flora fanerogámica Argentina, Fasc. 63: Hypochoeris L. ProFlora (Conicet),...
  • K. Bremer

    Asteraceae: Cladistics and Classification

    (1994)
  • K. Bremer

    Major clades and grades of the Asteraceae

  • K. Bremer et al.

    East Gondwana ancestry of the sunflower alliance of families

    Proc. Natl. Acad. Sci. USA

    (1997)
  • Cerbah, M., 1997. Heterochromatine, organisateurs nucléolaires et evolution du génome chez quelques espèces végétales:...
  • M. Cerbah et al.

    rDNA organization and evolutionary relationships in the genus Hypochaeris (Asteraceae)

    J. Hered.

    (1998)
  • M. Cerbah et al.

    Molecular phylogeny of the genus Hypochaeris using internal transcribed spacers of nuclear rDNA: inference for chromosomal evolution

    Mol. Biol. Evol.

    (1998)
  • M. Cerbah et al.

    Evolutionary DNA variation in the genus Hypochaeris

    Heredity

    (1999)
  • M. Coleman et al.

    Repeat intercontinental dispersal and Pleistocene speciation in disjunct Mediterranean and desert Senecio (Asteraceae)

    Am. J. Bot.

    (2003)
  • M.L. DeVore et al.

    The place and time of origin of the Asteraceae, with additional comments on the Calyceraceae and Goodeniaceae

  • J.J. Doyle et al.

    A rapid DNA isolation procedure for small quantities of fresh leaf tissue

    Phytochem. Bull.

    (1987)
  • J. Felsenstein

    Evolutionary trees from DNA sequences: a maximum likelihood approach

    J. Mol. Evol.

    (1981)
  • J. Felsenstein

    Confidence limits on phylogenies: an approach using the bootstrap

    Evolution

    (1985)
  • Felsenstein, J., 1995. PHYLIP (Phylogeny Inference Package), Version 3.57c. Univ. of Washington,...
  • J. Felsenstein

    Inferring Phylogenies

    (2004)
  • W.M. Fitch

    Toward defining the course of evolution: minimum change for a specific tree topology

    Syst. Zool.

    (1971)
  • A. Galán de Mera et al.

    Hypochaeris angustifolia (Asteraceae): distribución, ecología y fitosociología

    Acta Bot. Malacitana

    (1998)
  • A. Galán de Mera et al.

    Hypochaeris alliatae group (Asteraceae) in the western Mediterranean Region

    Nord. J. Bot.

    (1999)
  • A. Graham

    A contribution to the geologic history of the Compositae

  • T.A. Hall

    BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT

    Nucleic Acids Symp. Ser.

    (1999)
  • O. Hoffmann

    Hypochoeris L

  • E. Käss et al.

    Molecular phylogeny and phylogeography of Lupinus (Leguminosae) inferred from nucleotide sequences of the rbc L gene and ITS 1 + 2 regions of rDNA

    Plant Syst. Evol.

    (1997)
  • K.-J. Kim et al.

    Comparison of phylogenetic hypotheses among different data sets in dwarf dandelions (Krigia, Asteraceae): additional information from internal transcribed spacer sequences of nuclear ribosomal DNA

    Plant Syst. Evol.

    (1994)
  • K.-J. Kim et al.

    ndhF sequence evolution and the major clades in the sunflower family

    Proc. Natl. Acad. Sci. USA

    (1995)
  • S.-C. Kim et al.

    A common origin for woody Sonchus and five related genera in the Macaronesian islands: molecular evidence for extensive radiation

    Proc. Natl. Acad. Sci. USA

    (1996)
  • S.-C. Kim et al.

    Adaptive radiation and genetic differentiation in the woody Sonchus alliance (Asteraceae: Sonchinae) in the Canary Islands

    Plant Syst. Evol.

    (1999)
  • W.J.M. Koopman et al.

    Phylogenetic relationships among Lactuca (Asteraceae) species and related genera based on ITS-1 DNA sequences

    Am. J. Bot.

    (1998)
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