PHYLOGENY OF GAERTNERA LAM. (RUBIACEAE) BASED ON MULTIPLE DNA MARKERS: EVIDENCE OF A RAPID RADIATION IN A WIDESPREAD, MORPHOLOGICALLY DIVERSE GENUS
Simon T. Malcomber
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166–0299
Program of Evolutionary and Population Biology, Department of Biology, Washington University, St. Louis, Missouri 63130
Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121; E-mail: [email protected].
Search for more papers by this authorSimon T. Malcomber
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166–0299
Program of Evolutionary and Population Biology, Department of Biology, Washington University, St. Louis, Missouri 63130
Department of Biology, University of Missouri-St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121; E-mail: [email protected].
Search for more papers by this authorAbstract
Abstract Phylogenetic relationships among 28 of the 68 species of the paleotropical genus Gaertnera (Rubiaceae) and two related genera were inferred from nucleotide sequence variation in four nuclear DNA (nDNA) markers: the internal transcribed spacers of nuclear rDNA (ITS), the large and small copies of phosphoenolpyruvate carboxylase (PepC-large and PepC-small), and triose phosphate isomerase (Tpi). Phylogenetic analysis of the combined nDNA dataset suggested that Gaertnera is monophyletic, but genetic variation among species was insufficient to reconstruct well-supported relationships within the genus. This was counter to expectations based on the very distinct morphologies and widespread distribution of the genus (West Africa to Sulawesi). Molecular clock analyses suggested variable dates of origin for Gaertnera depending upon the calibration method used. The most plausible calibration implies that Gaertnera migrated to Africa during the early Tertiary, possibly via a boreotropical land bridge and suggests that Gaertnera started to radiate 5.21 ± 0.14 million years ago. This implies that range expansion in the group has occurred via a number of long-distance dispersal events rather than vicariance. The molecular clock estimate in turn estimated an unusually rapid lineage diversification rate within the radiation of 0.717–0.832 species/million years, comparable to those estimated for radiations on oceanic islands. Although low interspecific competition levels may have contributed to the diversification of Gaertnera on Mauritius, the mechanisms driving the rapid radiation of the group in other parts of its range remain elusive.
Literature Cited
- Andersson, L., and J. H. E. Rova. 1999. The rps16 intron and the phylogeny of the Rubioideae (Rubiaceae). Plant. Syst. Evol. 214: 161–186.
- Baldwin, B. G., and M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl. Acad. Sci. 95: 9402–9406.
- Baum, D. A., K. J. Sytsma, and P. C. Hoch. 1994. A phylogenetic analysis of Epilobium (Onagraceae) based on nuclear ribosomal DNA sequences. Syst. Bot. 19: 363–388.
- Baum, D. A., R. L. Small, and J. F. Wendel. 1998. Biogeography and floral evolution of baobabs (Adansonia, Bombacaeae) as inferred from multiple data sets. Syst. Biol. 47: 181–207.
- Bawa, K. S., D. R. Perry, S. H. Bullock, R. E. Colville, and M. H. Grayum. 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination mechanisms. Am. J. Bot. 72: 346–356.
- Boom, B. 1989. A new species of Pagamea (Rubiaceae) from Brazilian Guayana. Brittonia 41: 129–130.
- Bradshaw, H. D., Jr., S. M. Wilbert, K. G. Otto, and D. W. Schemske. 1995. Genetic mapping of floral traits associated with reproductive isolation in monkey flowers (Mimulus). Nature 376: 762–765.
- Bremer, B. 1996. Phylogenetic studies within Rubiaceae and relationships to other families based on molecular data. Opera Bot. Belg. 7: 33–50.
- Bremer, B., and O. Eriksson. 1992. Evolution of fruit characters and dispersal modes in the tropical family Rubiaceae. Biol. J. Linn. Soc. 47: 59–95.
- Buckler, E. S., A. Ippolito, and T. P. Holtsford. 1997. The evolution of ribosomal DNA: paralogues and phylogenetic implications. Genetics 145: 821–832.
- Carr, G. D., and D. W. Kyhos. 1981. Adaptive radiation in the Hawaiian silversword alliance (Compositae-Madiinae)I. Cytogenetics of spontaneous hybrids. Evolution 35: 543–556.
- Carson, H. L. 1970. Chromosome tracers of the origin of species. Science 168: 1414–1418.
- Cunningham, C. W. 1997. Can three incongruence tests predict when data should be combined Mol. Biol. Evol. 14: 733–740.
- Doebley, J., and A. Stec. 1991. Genetic analysis of the morphological differences between maize and teosinte. Genetics 129: 285–295.
- Doyle, J. A., and M. J. Donoghue. 1993. Phylogenies and angiosperm diversification. Paleobiology 19: 141–167.
- Doyle, J. J., and J. L. Doyle. 1987. A rapid isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11–15.
- Farris, J. S., M. Käellersjö, A. G. Kluge, and C. Bult. 1994. Testing significance of incongruence. Cladistics 10: 315–319.
- Felsenstein, J. 1985. Confidence limits of phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
- Felsenstein, J. 1988. Phylogenies from molecular sequences: inference and reliability. Annu. Rev. Genet. 22: 521–565.
- Felsenstein, J. 1995. PHYLIP. Ver. 3.57c. Dept. of Genetics, Univ. of Washington, Seattle , WA .
- Francisco-Ortega, J., D. J. Crawford, A. Santos-Guerva, and R. K. Janson. 1997. Origin and evolution of Argyranthemun (Asteridaceae: Anthermideae) in Macronesia. Pp. 407–431 in T. J. Givnish and K. J. Sytsma, eds. Molecular evolution and adaptive radiation. Cambridge Univ. Press, Cambridge , U.K.
- Freed, L. A., S. Conant, and R. C. Fleisher. 1987. Evolutionary ecology and radiation of the Hawaiian passerine birds. Trends Ecol. Evol. 2: 196–203.
- Goldman, N., J. P. Anderson, and A. G. Rodrigo. 2000. Likelihood-based tests of topologies in phylogenetics. Syst. Biol. 49: 652–670.
- Grant, P. R. 1986. Ecology and evolution of Darwin's finches. Princeton Univ. Press, Princeton , NJ .
- Hasegawa, M., H. Kishino, and T. Yano. 1985. Dating of the humanape splitting by molecular clock. J. Mol. Evol. 22: 160–174.
- Heilbuth, J. C. 2000. Lower species richness in dioecious clades. Am. Nat. 156: 221–241.
- Hillis, D. M., and J. P. Huelsenbeck. 1992. Signal, noise, and reliability in molecular phylogenetic analysis. J. Hered. 83: 189–195.
- Hodges, S. A., and M. A. Arnold. 1994. Columbines: a geographically widespread species flock. Proc. Natl. Acad. Sci. 91: 5129–5132.
- Hodges, S. A., and M. A. Arnold. 1995. Spurring plant diversification: Are floral nectar spurs a key innovation Proc. R. Soc. Lond. B 262: 343–348.
- Holmgren, P. K., N. H. Holmgren, and L. Barnett. 1990. Index herbariorum. Part I. The herbaria of the world. 8th ed. New York Botanical Garden, New York .
- Igersheim, A., C. Puff, P. Leins, and C. Erbar. 1994. Gynocial development of Gaertnera Lam. and of presumably allied taxa of the Psychotrieae (Rubiaceae): secondarily “superior” vs. inferior ovaries. Bot. Jahrb. Syst. 116: 401–414.
- Jansen, S., E. Robbrecht, H. Beeckman, and E. Smets. 1996. Gaertnera and Pagamea: genera within the Psychotrieae or constituting the tribe Gaertnereae? A wood anatomical and palynological approach. Bot. Acta 109: 466–476.
- Jensen, J. S. 1990. Plausability and testability, assessing the consequences of evolutionary innovations. Pp. 171–190 in M. Nitecki, ed. Evolutionary innovations. Univ. of Chicago Press, Chicago , IL .
-
Johnson, L. A., and
D. E. Soltis. 1998. Assessing congruence: empirical examples from molecular data. Pp.
297–343
in
D. E. Soltis,
P. S. Soltis, and
J. J. Doyle, eds.
Molecular systematics of plants. II. DNA sequencing. Kluwer Academic Press,
Boston
,
MA
.
10.1007/978-1-4615-5419-6_11 Google Scholar
- Kellogg, E. A. 2000. A model of inflorescence development. Pp. 84–88 in K. L. Wilson and D. A. Morrison, eds. Monocots: systematics and evolution. CSIRO, Melbourne .
- Lack, D. 1947. Darwin's finches. Cambridge Univ. Press, Cambridge , U.K.
- Larson, A. 1994. The comparison of morphological and molecular data in phylogenetic systematics. Pp. 371–390 in B. Schierwater, B. Streit, G. P. Wagner, and R. DeSalle, eds. Molecular ecology and evolution: approaches and applications. Birkhauser Verlag, Basel , Switzerland .
- Li, W.-H., and D. Grauer. 1991. Fundamentals of molecular evolution. Sinauer, Sunderland , MA .
- Liem, K. F. 1990. Key evolutionary innovations, differential diversity, and symecomorphosis. Pp. 147–170 in M. Nitecki, ed. Evolutionary innovations. Univ. of Chicago Press, Chicago , IL .
- MacDougal, I., and F. H. Chauman. 1969. Isotopic dating and geomagnetic polarity studies on volcanic rocks from Mauritius, Indian Ocean. Geol. Soc. Am. Bull. 80: 1419–1442.
- Malcomber, S. T. 2000. Systematics and the evolution of breeding systems in Gaertnera Lam. (Rubiaceae). Ph.D. diss., Washington University in St. Louis, St. Louis, MO.
- Meyer, A., T. D. Kocher, and A. C. Wilson. 1990. Monophyletic origin of Lake Victoria cichlid fishes suggested by mitochondrial DNA sequences. Nature 347: 550–553.
- Pailler, T., and J. D. Thompson. 1997. Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Reunion Island. Am. J. Bot. 84: 315–327.
- Parrish, J. T. 1993. The paleogeography of the opening South Atlantic. Pp. 8–27 in W. George and R. Lavocat, eds. The Africa-South America connection. Oxford Univ. Press, Oxford , U.K.
- Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14(9): 817–818.
- Rambaut, A. 1996. Se-Al vers.1.d1. Available via ftp:evolve.zo.ox.ac.ukpackagesSe-A1Se-A110a1.hqx.
- Rice, W. R. 1989. Analyzing tables of statistical tests. Evolution 43: 223–225.
- Richards, P. W. 1996. The tropical rainforest: an ecological study. 2d. ed. Cambridge Univ. Press, Cambridge , U.K.
- Roth, J. L., and D. L. Dilcher. 1979. Investigations of angiosperms from the Eocene of North America: stipulate leaves of the Rubiaceae. Am. J. Bot. 66: 1194–1207.
-
Sambrook, J. C.,
E. F. Fritsch, and
T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Lab. Press,
Cold Spring Harbor
,
NY
.
10.1111/j.1095-8312.1996.tb01434.x Google Scholar
-
Sanderson, M. J.
1998. Estimating rate and time in molecular phylogenies: beyond the molecular clock??
Pp.
242–264
in
D. E. Soltis,
P. S. Soltis, and
J. J. Doyle, eds.
Molecular systematics of plants. II. DNA sequencing. Kluwer Academic,
Boston
,
MA
.
10.1007/978-1-4615-5419-6_9 Google Scholar
- Sanderson, M. J., and M. J. Donoghue. 1996. Reconstructing shifts in diversification rates on phylogenetic trees. Trends Ecol. Evol. 11: 15–20.
- Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114–1116.
- Strand, A. E., J. Leebens-Mack, and B. G. Milligan. 1997. Nuclear DNA-based markers for plant evolutionary biology. Mol. Ecol. 6: 113–118.
- Steyermark, J. A. 1965. Pagamea. Pp. 270–285 in B. Maguire et al., eds. Botany of the Guayana Highland. Part VI. Mem. NY Bot. Gard. 12:1–285.
- Suh, Y., L. B. Thein, H. E. Reeve, and E. A. Zimmer. 1993. Molecular evolution and phylogenetic implications of internal transcribed spacer sequences of ribosomal DNA in Winteraceae. Am. J. Bot. 80: 1042–1055.
- Swofford, D. L. 2000. PAUP*: phylogenetic analysis using parsimony. Ver. 4.0b. Sinauer Associates, Sunderland , MA .
- Taberlet, P. L., L. Gielly, G. Pautou, and J. Bouvet. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol. Biol. 17: 1105–1109.
- Templeton, A. R. 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution 37: 221–244.
- Thompson, J., T. Gibson, and D. Higgins. 1994. Clustal W, version 1.7: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673–4680.
- Tiffney, B. H. 1985. The Eocene North Atlantic land bridge: its importance in Tertiary and modern phytogeography of the Northern hemisphere. J. Arnold Arbor. 66: 243–273.
- van Beusekom, C. F. 1968. A revision of the Malesian and Ceylonese species of the genus Gaertnera Lamk. (Rubiaceae). Blumea 15: 359–391.
- Wendel, J. F., A. Schnabel, and T. Seelanan. 1995. An unusual ribosomal sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. Mol. Phylogenet. Evol. 4: 298–313.
- White, T. J., T. Birns, S. Lee, and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pp. 315–322 in M. Innis, D. Gelfand, J. Sninsky, and T. White, eds. PCR protocols: a guide to methods and applications. Academic Press, San Diego , CA .