Download PDF
Plant Biol (Stuttg) 2004; 6(4): 477-490
DOI: 10.1055/s-2004-817909
Original Paper

Georg Thieme Verlag Stuttgart KG · New York

Evolution of Carnivory in Lentibulariaceae and the Lamiales

K. Müller1 , T. Borsch1 , L. Legendre2 , S. Porembski3 , I. Theisen1 , W. Barthlott1
  • 1Nees-Institute for Biodiversity of Plants, University of Bonn, Bonn, Germany
  • 2Centre for Horticulture and Plant Sciences, University of Western Sydney, Sydney, Australia
  • 3Institut für Biodiversitätsforschung, Allgemeine und Spezielle Botanik, Universität Rostock, Wismarsche Straße 8, 18051 Rostock, Germany
Further Information

Publication History

Publication Date:
12 July 2004 (online)

   Permissions and Reprints

Abstract

As a basis for analysing the evolution of the carnivorous syndrome in Lentibulariaceae (Lamiales), phylogenetic reconstructions were conducted based on coding and non-coding chloroplast DNA (matK gene and flanking trnK intron sequences, totalling about 2.4 kb). A dense taxon sampling including all other major lineages of Lamiales was needed since the closest relatives of Lentibulariaceae and the position of “proto-carnivores” were unknown. Tree inference using maximum parsimony, maximum likelihood, and Bayesian approaches resulted in fully congruent topologies within Lentibulariaceae, whereas relationships among the different lineages of Lamiales were only congruent between likelihood and Bayesian optimizations. Lentibulariaceae and their three genera (Pinguicula, Genlisea, and Utricularia) are monophyletic, with Pinguicula being sister to a Genlisea-Utricularia clade. Likelihood and Bayesian trees converge on Bignoniaceae as sister to Lentibulariaceae, albeit lacking good support. The “proto-carnivores” (Byblidaceae, Martyniaceae) are found in different positions among other Lamiales but not as sister to the carnivorous Lentibulariaceae, which is also supported by Khishino-Hasegawa tests. This implies that carnivory and its preliminary stages (“proto-carnivores”) independently evolved more than once among Lamiales. Ancestral states of structural characters connected to the carnivorous syndrome are reconstructed using the molecular tree, and a hypothesis on the evolutionary pathway of the carnivorous syndrome in Lentibulariaceae is presented. Extreme DNA mutational rates found in Utricularia and Genlisea are shown to correspond to their unusual nutritional specialization, thereby hinting at a marked degree of carnivory in these two genera.

Key words

Carnivorous plants - Lamiales - Lentibulariaceae - matK-trnK - molecular phylogeny - mutation rates.

References

  • 1 Albach D. C., Soltis P. S., Soltis D. E., Olmstead R. G.. Phylogenetic analysis of asterids based on sequences of four genes.  Annals of the Missouri Botanical Garden. (2001);  88 163-212
    PubMedGoogle Scholar
  • 2 Albert V. A., Williams S. E., Chase M. W.. Carnivorous plants: Phylogeny and structural evolution.  Science. (1992);  257 1491-1495
    PubMedGoogle Scholar
  • 3 Barraclough T. G., Savolainen V.. Evolutionary rates and species diversity in flowering plants.  Evolution. (2001);  55 677-683
    PubMedGoogle Scholar
  • 4 Barthlott W., Porembski S., Fischer E., Gemmel B.. First protozoa-trapping plant found.  Nature. (1998);  392 447
    PubMedGoogle Scholar
  • 5 Borsch T.. Phylogeny and Evolution of the genus Nymphaea (Nymphaeaceae). PhD Thesis. Bonn; University of Bonn (2000)
    Google Scholar
  • 6 Borsch T., Hilu K. W., Quandt D., Wilde V., Neinhuis C., Barthlott W.. Non-coding plastid trnT-trnF sequences reveal a well supported phylogeny of basal angiosperms.  Journal of Evolutionary Biology. (2003);  16 558-576
    CrossrefPubMedGoogle Scholar
  • 7 Bremer B., Bremer K., Heidari N., Erixon P., Olmstead R. G.. Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels.  Molecular Phylogenetics and Evolution. (2002);  24 274-301
    CrossrefPubMedGoogle Scholar
  • 8 Britten R. J.. Rates of DNA sequence evolution differ between taxonomic groups.  Science. (1986);  231 1393-1398
    PubMedGoogle Scholar
  • 9 Casper S. J.. Monographie der Gattung Pinguicula L.  Bibliotheca Botanica. (1966);  127/128 1-209
    PubMedGoogle Scholar
  • 10 Darwin C.. Insectivorous Plants. London; Murray (1875)
    Google Scholar
  • 11 Dixon K. W., Pate J. S., Bailey W. J.. Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves.  Australian Journal of Botany. (1980);  28 283-297
    PubMedGoogle Scholar
  • 12 Doyle J. A., Bygrave P., Le Thomas A.. Implications of molecular data for pollen evolution in Annonaceae. Harley, M. M., Morton, C. M., and Blackmore, S., eds. Pollen and Spores: Morphology and Biology. Kew; Royal Botanical Gardens (2000): 259-284
    Google Scholar
  • 13 Farris J. S., Albert V. A., Källersjö M., Lipscomb D., Kluge A. G.. Parsimony Jackknifing outperforms Neighbor-Joining.  Cladistics. (1996);  12 99-124
    CrossrefPubMedGoogle Scholar
  • 14 Fischer E., Porembski S., Barthlott W.. Revision of the genus Genlisea (Lentibulariaceae) in Africa and Madagascar with notes on ecology and phytogeography.  Nordic Journal of Botany. (2000);  20 291-318
    PubMedGoogle Scholar
  • 15 Fromm-Trinta E.. Tayloria Fromm-Trinta - Nova Seca do genere Genlisea St.-Hil.  Boletin Museum Nacional de Rio de Janeiro, Botanica. (1977);  44 1-4
    PubMedGoogle Scholar
  • 16 Hilu K. W., Liang H.. The matK gene: Sequence variation and application in plant systematics.  American Journal of Botany. (1997);  87 830-839
    PubMedGoogle Scholar
  • 17 Hilu K. W., Borsch T., Müller K., Soltis D. E., Soltis P. S., Savolainen V., Chase M. W., Powell M. P., Alice L. A., Evans R., Sauquet H., Neinhuis C., Slotta T. A. B., Rohwer J. G., Campbell C. S., Chatrou L. W.. Angiosperm phylogeny based on matK sequence information.  American Journal of Botany. (2003);  90 1758-1776
    PubMedGoogle Scholar
  • 18 Huelsenbeck J. P.. Performance of phylogenetic methods in simulation.  Systematic Biology. (1995);  44 17-48
    PubMedGoogle Scholar
  • 19 Huelsenbeck J. P., Ronquist F.. MrBayes: Bayesian inference of phylogenetic trees.  Bioinformatics. (2001);  17 754-755
    CrossrefPubMedGoogle Scholar
  • 20 Huelsenbeck J. P., Larget B., Miller R. E., Ronquist F.. Potential applications and pitfalls of Bayesian inference of phylogeny.  Systematic Biology. (2002);  51 673-688
    CrossrefPubMedGoogle Scholar
  • 21 Jobson R. W., Albert V. A.. Molecular rates parallel diversification contrasts between carnivorous plant sister lineages.  Cladistics. (2002);  18 127-136
    PubMedGoogle Scholar
  • 22 Johnson L. A., Soltis D. E.. Phylogenetic inference in Saxifragaceae s.str. and Gilia (Polemoniaceae) using matK sequences.  Annals of the Missouri Botanical Garden. (1995);  82 149-175
    PubMedGoogle Scholar
  • 23 Juniper B. E.. The Path to Plant Carnivory. Juniper, B. E. and Southwood, R., eds. Insects and the Plant Surface. London; Echvard Annald (1986)
    Google Scholar
  • 24 Juniper B. E., Robins R. J., Joel D. M.. The Carnivorous Plants. London; Academic Press (1989)
    Google Scholar
  • 25 Kelchner S. A.. The evolution of noncoding chloroplast DNA and its application in plant systematics.  Annals of the Missouri Botanical Garden. (2000);  87 482-498
    PubMedGoogle Scholar
  • 26 Kishino H., Hasegawa M.. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea.  Journal of Molecular Evolution. (1989);  29 170-179
    PubMedGoogle Scholar
  • 27 Kron K. A., Fuller R., Crayn D. M., Gadek P. A., Quinn C. J.. Phylogenetic relationships of epacrids and vaccinioids (Ericaceae s.l.) based on matK sequence data.  Plant Systematics and Evolution. (1999);  218 55-65
    CrossrefPubMedGoogle Scholar
  • 28 Legendre L.. The genus Pinguicula L. (Lentibulariaceae): an overview.  Acta Botanica Gallica. (2000);  147 77-95
    PubMedGoogle Scholar
  • 29 Lewis P. O.. Maximum likelihood as an alternative tp parsimony for inferring phylogeny using nucleotide sequence data. Soltis, D. S. et al., eds. Molecular Systematics of Plants II: DNA Sequencing. Boston; Kluwer (1998): 132-163
    Google Scholar
  • 30 Liang H. P., Hilu K. W.. Application of the matK gene to grass systematics.  Canadian Journal of Botany. (1996);  74 125-134
    PubMedGoogle Scholar
  • 31 Lloyd F. E.. Carnivorous plants. In Chronica Botanica Co. Massachusetts; Waltham (1942)
    Google Scholar
  • 32 Lüttge U.. Ecophysiology of carnivorous plants. Lange, O. L. et al., eds. Physiological Plant Ecology III. Berlin, Heidelberg; Springer (1983)
    Google Scholar
  • 33 Maddison W. P., Maddison D. R.. MacClade. Sunderland, MA; Sinauer (1992)
    Google Scholar
  • 34 Marschner H.. Mineral Nutrition of Higher Plants, 2nd ed. New York; Academic Press (1995)
    Google Scholar
  • 35 Martin A. P., Palumbi S. R.. Body size, metabolic rate, generation time, and the molecular clock.  Proceedings of the National Academy of Sciences USA. (1993);  90 4087-4091
    PubMedGoogle Scholar
  • 36 Meimberg H., Wistuba A., Dittrich P., Heubl G.. Molecular phylogeny of Nepenthaceae based on cladistic analysis of plastid trnK intron sequence data.  Plant Biology. (2001);  3 164-175
    Article in Thieme ConnectPubMedGoogle Scholar
  • 37 Mishler B. D.. The cladistic analysis of molecular and morphological data.  American Journal of Physical Anthropology. (1994);  94 143-156
    PubMedGoogle Scholar
  • 38 Mohr G., Perlman P. S., Lambowitz A. M.. Evolutionary relationships among group II intron-encoded proteins and identification of a conserved domain that may be related to maturase function.  Nucleic Acids Research. (1993);  21 4991-4997
    PubMedGoogle Scholar
  • 39 Müller J., Müller K.. QuickAlign: a new alignment editor.  Plant Mol. Biol. Reporter. (2003);  21 5
    PubMedGoogle Scholar
  • 40 Müller K.. PRAT: Computer program for phylogenetic analysis of large data sets. Bonn; Program distributed by the author (2002)
    Google Scholar
  • 43 Neuhaus H., Link G.. The chloroplast tRNALys (UUU) gene from mustard (Sinapis alba) contains a class II intron potentially coding for a maturase related polypeptide.  Current Genetics. (1987);  11 251-257
    CrossrefPubMedGoogle Scholar
  • 44 Nickrent D. L., DePamphilis C. W., Wolfe A. D.. Molecular phylogenetic and evolutionary studies of parasitic plants. Soltis, D. S. et al., eds. Molecular Systematics of Plants II: DNA Sequencing. Boston; Kluwer (1998): 211-241
    Google Scholar
  • 45 Nixon K. C.. The Parsimony Ratchet, a new method for rapid parsimony analysis.  Cladistics. (1999);  15 407-414
    PubMedGoogle Scholar
  • 46 Olmstead R. G., Reeves P. A.. Evidence for the polyphyly of the Scrophulariaceae based on chloroplast rbcL and ndhF sequences.  Annals of the Missouri Botanical Garden. (1995);  82 176-193
    PubMedGoogle Scholar
  • 47 Olmstead R. G., DePamphilis C. W., Wolfe A. D., Young N. D., Elisons W. J., Reeves P. A.. Disintegration of the Scrophulariaceae.  American Journal of Botany. (2001);  88 348-361
    PubMedGoogle Scholar
  • 48 Oxelman B., Backlund M., Bremer B.. Relationships of the Buddlejaceae s.l. investigated using parsimony jackknife and branch support analysis of chloroplast ndhF and rbcL sequence data.  Systematic Botany. (1999);  24 164-182
    PubMedGoogle Scholar
  • 49 Posada D., Crandall K. A.. Modeltest: testing the model of DNA substitution.  Bioinformatics. (1998);  14 817-818
    CrossrefPubMedGoogle Scholar
  • 50 Pringsheim E. G., Pringsheim O.. Kleiner Beitrag zur Physiologie von Utricularia. .  Zeitschrift für Pflanzenphysiologie. (1967);  57 1-10
    PubMedGoogle Scholar
  • 52 Rutishauser R., Sattler R.. Complementary and heuristic value of contrasting models in structural botany. III. Case study on shoot-like “leaves” and leave-like “shoots” in Utricularia macrorhiza und U. purpurea (Lentibulariaceae).  Botanische Jahrbücher für Systematik, Pflanzengeschichte und Pflanzengeographie. (1989);  111 121-137
    PubMedGoogle Scholar
  • 53 Savolainen V., Chase M. W., Hoot S. B., Morton C. M., Soltis D. E., Bayer C., Fay M. F., De Bruijn A. Y., Sullivan S., Qiu Y.-L.. Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences.  Systematic Biology. (2000);  49 306-362
    PubMedGoogle Scholar
  • 54 Schnepf E.. Struktur und Funktion der Golgi-Elemente in Insektivoren-Drüsen.  Berichte der Deutschen Botanischen Gesellschaft. (1961);  74 269
    PubMedGoogle Scholar
  • 55 Seine R., Porembski S., Balduin M., Theisen I., Wilbert N., Barthlott W.. Different prey strategies of terrestrial and aquatic species in the carnivorous genus Utricularia (Lentibulariaceae).  Botanische Jahrbücher für Systematik. (2002);  124 71-76
    PubMedGoogle Scholar
  • 56 Soltis D. E., Soltis P. S., Chase M. W., Mort M. E., Albach D. C., Zanis M., Savolainen V., Hahn W. H., Hoot S. B., Fay M. F., Axtell M., Swensen S. M., Prince L. M., Kress W. J., Nixon K. C., Farris J. S.. Angiosperm phylogeny inferred from 18S rDNA, rbcL, and atpB sequences.  Botanical Journal of the Linnaean Society. (2000);  133 381-461
    PubMedGoogle Scholar
  • 57 Spomer G.. Evidence of protocarnivorous capabilities in Geranium viscosisimum and Potentilla arguta and other sticky plants.  International Journal of Plant Sciences. (1999);  160 98-101
    CrossrefPubMedGoogle Scholar
  • 58 Steele K. P., Vilgalys R.. Phylogenetic analyses of Polemoniaceae using nucleotide sequences of the plastid gene matK. .  Systematic Botany. (1994);  19 126-142
    PubMedGoogle Scholar
  • 59 Suzuki Y., Glazko G. V., Nei M.. Overcredibility of molecular phylogenetics obtained by Bayesian phylogenetics.  Proceedings of the National Academy of Sciences, USA. (2002);  99 16138-16143
    CrossrefPubMedGoogle Scholar
  • 60 Swofford D. L., Olsen G. J., Waddell P. J., Hillis D.. Phylogenetic inference. Hillis, D. M., Moritz, C., and Mable, B. K., eds. Molecular Systematics, 2nd edition. Sunderland, MA; Sinauer Associates (1996): 407-514
    Google Scholar
  • 61 Swofford D. L.. PAUP*. Phylogenetic Analysis Using Parsimony (*and other Methods). Sunderland; Sinauer Associates (1998)
    Google Scholar
  • 62 Taylor P.. The Genus Utricularia: A Taxonomic Monograph. London; Kew Bulletin Additional Series XIV (1989)
    Google Scholar
  • 63 Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.  Nucleic Acids Research. (1997);  24 4876-4882
    PubMedGoogle Scholar
  • 64 Vogel J., Hübschmann T., Börner T., Hess W. R.. Splicing and intron-internal RNA editing of trnK-matK transcripts in barley plastids: support for matK as an essential splice factor.  Journal of Molecular Biology. (1997);  270 179-187
    CrossrefPubMedGoogle Scholar
  • 65 Wu C. I., Li W. H.. Evidence for higher rates of nucleotide substitution in rodents than in man.  Proceedings of the National Academy of Sciences, USA,. (1985);  82 1741-1745
    PubMedGoogle Scholar
  • 66 Young N. D., Steiner K. E., DePamphilis C. W.. The evolution of parasitism in Scrophulariaceae/Orobanchaceae: Plastid gene sequences refute an evolutionary transition series.  Annals of the Missouri Botanical Garden. (1999);  86 876-893
    PubMedGoogle Scholar
  • 67 Young N. D., DePamphilis C. W.. Purifying selection detected in the plastid gene matK and flanking ribozyme regions within a group II intron of nonphotosynthetic plants.  Molecular Biology and Evolution. (2000);  17 1933-1941
    PubMedGoogle Scholar
  • 68 Ziegler H., Lüttge U.. Über die Resorption von 14C-Glutaminsäure durch sezernierende Nektarien.  Naturwissenschaften. (1959);  46 176-177
    PubMedGoogle Scholar

K. Müller

Nees-Institut für Biodiversität der Pflanzen
Friedrich-Wilhelms-Universität Bonn

Meckenheimer Allee 170

53115 Bonn

Germany

Email: kaimueller@uni-bonn.de

Section Editor: K. Clay

      >