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Molecular Phylogeny of the Genus Phaseolus L. (Fabaceae)

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Molecular Phylogeny of the Genus Phaseolus L. (Fabaceae) 31 Molecular Phylogeny of the Genus Phaseolus L. (Fabaceae) A. Delgado-Salinas^, R. Bibler^ and M. Lavin ^ ^Instituto de Biología, UNAM, México, D. F. México ^Plant Science and Plant Pathology, Montana State University, Bozeman, Montana Introduction This study was designed to determine the closest relatives of Phaseolus using nucleotide sequences from the cpDNA trnK and nrDNA ITS/5.8S regions, as well as morphological data. Such data were utilized because they have been shown to be phylogenetically informative in legumes (e.g., Delgado-Salinas et al. 1999; Lavin et al. 2003; Riley-Hultmg et al. 2004; Thulin et al, in press). The goals of this study thus include a systematic and phylogenetic analysis of the genus Phaseolus^ which addresses the relationships of the species, the identity of species groups within the genus, as well as the relationships of the genus to other neotropical genera. We also explored the various ways these phylogenies can be used to answer questions about the age of diversification oí Phaseolus species, and the evolution of their characters. The development of a well-supported and informative phylogeny should also facilitate breeding programs by more accurately determining membership in primary and higher order gene pools. Results and Discussion Using DNA sequence data from the chloroplast gene trnK (which includes matk) and the internal transcribed spacer region (ITS) of the nuclear ribosomal RNA genes, a molecular phylogeny oí Phaseolus was constructed via parsimony and Bayesian likelihood methods. The combined analysis of two genetic loci and morphological characters corroborated the previously detected monophyly of the genus, but more definitively placed it as sister to the rest of the New World Phaseolinae genera, which includes Macroptilium, Mysanthus, Oryxis, Oxyrhynchus, Ramirezella, Strophostyles^ and the neotropical species of Vigna excluding the species of subgenus Lasiospron. In essence, Phaseolus represents an isolated basally branching lineage within the New World radiation of Phaseolinae. This study combining two genetic loci and morphological data also more accurately determined the phylogenetic relationships among Phaseolus species than did the study of Delgado-Salinas et al. (1999), which relied strictly on ITS sequences and morphological data for phylogenetic inference. Some Phaseolus specits clades were supported in both analyses and these groups also corresponded to the subgeneric classification of Phaseolus proposed by Freytag and Debouck (2002). Clades resolved in the combined phylogeny, such as one comprising P. microcarpus, P. glabellus and P. oaxacanus, were surprising because they seeming conflicted with the ITS tree (Delgado-Salinas et al. 1999). However, this putative conflict was really the result of poor clade support for certain of the ITS clades resolved in Delgado-Salinas (1999). Other instances of conflict between the combined analysis including cpDNA trnK and that with just the nrDNA ITS region included the conflicting positions of P. vulgaris, P. coccineus, and P.dumosus, which may Qxplain the hybrid origins of the last, as discussed in Delgado-Salinas et al. (1999, p. 448), where the evolution oí Phaseolus was hypothesized to be complex and potentially involve some reticulate evolution. 32 The combined phylogenetic analysis also revealed the taxonomic limitations of certain morphological character states. Many of the morphological differences among taxa have arisen multiple times, and appear to reflect adaptation to particular habitats rather than shared phylogenetic history. For example, the manner of germination, root type, and stigma position have carried much taxonomic weight in the past, but are nov^ realized to be much more prone to convergent evolution that previously thought. The new classifications of the species of Phaseolus will have to abandon or down weight these traditionally important characters. In addition, the age of the diversification of the modem species oí Phaseolus was estimated at pre-Pleistocene, or 4.5 Ma as estimated with the penalized likelihood method (Sanderson, 2002). This method also revealed a relatively fast rate of evolution for the tmK locus in Phaseolus, In particular, the matK coding region has an estimated substitution rate that ranges 4.7-6.9 x 10"^^ substitution per site per year, which is about the fastest rate estimated for all legume subgroups (Lavin et al., in prep.). This strongly suggests that the lack of molecular divergence among the South American species oí Phaseolus is a result of these species migrating out of an originally Mesoamerican distribution, where present-day genetic diversity is high, and into their present southern hemisphere geographical range. Finally, there is disagreement among certain of the phylogenetic relationships resolved with our combined molecular analyses and those depicted in the classification recently proposed by Freytag and Debouck (2002). This is mostly due, however, to Freytag and Debouck*s classification that does not adhere to the phylogenetic tenets of classification, such as using the criterion of monophyly to formally recognize taxonomic groups. References: Delgado-Salinas, A., T. Turley, A. Richman, and M. Lavin. 1999. Phylogenetic analysis of the cultivated and wild species oí Phaseolus (Fabaceae). Systematic Botany 23(3): 438-460. Freytag, G.F. and D. G. Debouck. 2002. Taxonomy, Distribution, and Ecology of the genus Phaseolus (Leguminosae - Papilionoideae) in North America, Mexico and Central America. Sida, Botanical Miscellany No. 23:1 -300. Lavin, M., M. F. Wojciechowski, P. Gasson, G. Hughes, and E. Wheeler. 2003. Phylogeny of robinioid legumes (Fabaceae) revisited: Coursetia and Gliricidia recircumscribed, and a biogeographical appraisal of the Caribbean endemics. Systematic Botany 28: 387-409. Lavin, M, M. F. Wojciechowski, and P. H. Herendeen. In prep. Evolutionary rates analysis of Leguminosae implicates a rapid diversification of the major family lineages immediately following an Early Tertiary emergence. To be submitted to Molecular Biology and Evolution. Riley-Hulting, E.T., A. Delgado-Salinas, and M. Lavin. 2004. Phylogenetic systematics of Strophostyles (ÇdbdiCQ^é): a North American temperate genus within a neotropical diversification. Systematic Botany 29(3). Sanderson, M. J. 2002. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Molecular Biology and Evolution 19: 101-109. Thulin, M., M. Lavin, R. Pasquet, and A. Delgado-Salinas. In press. Phylogeny and biogeography of Wajira (Leguminosae): a monophyletic segregate of Vigna centered in the Horn of Africa region. Systematic Botany (accepted). .
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