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Molecular Phylogenetics and Taxonomy of the Genus Thysanocarpus (Brassicaceae)

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Molecular Phylogenetics and Taxonomy of the Genus Thysanocarpus (Brassicaceae) Systematic Botany (2010), 35(3): pp. 1–19 © Copyright 2010 by the American Society of Plant Taxonomists Molecular Phylogenetics and Taxonomy of the Genus Thysanocarpus (Brassicaceae) Patrick J. Alexander , 1 , 4 Michael D. Windham , 2 Rajanikanth Govindarajulu , 1 Ihsan A. Al-Shehbaz , 3 and C. Donovan Bailey 1 1 BiologyProof Department, MSC 3AF, New Mexico State University,Only Las Cruces, New Mexico 88003, U. S. A. 2 Department of Biology, 139 Biological Sciences (Box 90338). Duke University, Durham, North Carolina 27708, U. S. A. 3 Department of Asian Botany, Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166, U. S. A. 4 Author for correspondence ( [email protected] ); first and second authors contributed equally. Communicating Editor: Daniel Potter Abstract— The relationships and taxonomy of the genus Thysanocarpus (Brassicaceae) are reassessed based on molecular phylogenetic analy- ses of nuclear ribosomal (ITS) and chloroplast ( trnL-F ) sequences and a critical re-examination of morphology and nomenclatural types. Based on these results, Thysanocarpus is well-supported as a member of tribe Thelypodieae, but no illuminating phylogenetic structure is found within the tribe. The independent origin of similar fruit morphology in Thysanocarpus and Athysanus is confirmed. Within Thysanocarpus , seven species are recognized: T. conchuliferus, T. curvipes, T. desertorum, T. erectus, T. laciniatus, T. radians , and T. rigidus comb. nov. Thysanocarpus lac- iniatus is found to have originated through hybridization. However, T. desertorum and T. rigidus , which have previously been included within T. laciniatus (as T. laciniatus var. hitchcockii and T. laciniatus var. rigidus , respectively), do not share that species’ hybrid origin and are dis- tinct both phylogenetically and morphologically. Within T. curvipes , five subspecies are recognized: T. curvipes subsp. amplectens comb. nov., T. curvipes subsp. curvipes , T. curvipes subsp. elegans comb. nov., T. curvipes subsp. longistylus comb. nov., and T. curvipes subsp. eradiatus comb. Nov. Thysanocarpus curvipes subsp. elegans and T. curvipes subsp. longistylus form clades in ITS and/or trnL-F cladograms as well as showing morphological distinction. The remaining three subspecies are recognized based on a combination of morphology and geography. Keywords— Fruit morphology , hybrid speciation , nuclear ribosomal ITS , Thelypodieae, trnL-F . Thysanocarpus Hook. is a genus of annuals in the fam- to Thysanocarpus ( Bailey et al. 2006 ; Mummenhoff et al. 2005 ; ily Brassicaceae, found from extreme southwestern British Warwick et al. 2008 ). Columbia south through the western United States to north- The goals of the present study are threefold. First, a family- western Mexico. The genus is most diverse in California, wide phylogenetic analysis is presented to test the mono- where all but one of the species ( T. erectus S. Wats., a Baja phyly of Thysanocarpus and establish its position within California endemic) are found. In the most recent synoptic Brassicaceae, including further confirmation of the separation treatment of the genus, Rollins (1993) recognized five species of Thysanocarpus and Athysanus . Second, infrageneric phylo- with no named infraspecific taxa. However, variation within genetic analyses within Thysanocarpus are used to refine our several of these taxa is substantial, and in the earlier treat- understanding of the number of taxa in the genus and their ment of California taxa, Munz (1959) recognized four variet- relationship with each other. Third, a revised taxonomy of the ies within T. curvipes Hook. and five within T. laciniatus Nutt. genus is presented based on both the results of infrageneric ex Torr. & A. Gray. Thysanocarpus is currently placed in the phylogenetic analyses and a re-examination of morphology. tribe Thelypodieae (formerly Schizopetaleae; see Beilstein et al. 2008 and Warwick et al. 2009 ) based on morphological and molecular phylogenetic investigations ( Bailey et al. 2006 ; Materials and Methods Al-Shehbaz et al. 2006 ; Alexander et al. 2006 ). Taxon Sampling and DNA Isolation— Leaf material for phylogenetic Thysanocarpus is notable for its unusual fruits, which are analysis of Thysanocarpus was obtained from recent collections and from orbicular to obovate winged silicles, unilocular, one-seeded, herbarium specimens from the following institutions: CAS, DS, JEPS, MO, NMC, RSA, and UC (see Appendix 1). Specimens were chosen to and indehiscent. These fruits may be glabrous or pubescent include multiple samples of all taxa recognized in treatments of the genus with simple, blunt-tipped trichomes. The only other species by Rollins (1993) and Munz (1959) and to include as much of the mor- in the western United States with similar fruits is Athysanus phological variation within T. curvipes and T. laciniatus as possible. A total pusillus (Hook.) Greene, which differs from Thysanocarpus in of 55 specimens of Thysanocarpus were used, including 29 specimens of the following respects: 1) the silicles are pubescent with unci- T. curvipes ; the geographic distribution of these samples is provided in Figs. 1 and 2 . DNA was isolated following the procedures of Alexander F1 F2 nate trichomes; 2) the silicles are borne in secund infructes- et al. (2007) , except that 10 m m Tris-HCl in 70% EtOH was used instead cences; and 3) the foliage is pubescent with branched of 70% EtOH when washing contaminants from the silica columns trichomes. Fruit similarities led A. pusillus to be named ini- at step 13. tially as a species of Thysanocarpus ( Hooker 1836 ). However, a To assess the monophyly of Thysanocarpus and its placement within Brassicaceae, we selected 51 samples of the family from GenBank for careful reexamination of morphology ( Al-Shehbaz et al. 2006 ) which both ITS and trnL-F spacer sequences were available. Sequences in conjunction with preliminary molecular phylogenetic anal- were chosen to sample broadly across the named tribes of Brassicaceae yses ( Alexander et al. 2006 ; see also Results) suggests an affili- and include as many species of tribe Thelypodieae as possible (tribes fol- ation with members of Arabideae and no particularly close low Al-Shehbaz et al. 2006 , Al-Shehbaz and Warwick 2007 ; Warwick et al. relationship with Thysanocarpus . Outside of North America 2009 ) The complete list of accessions is provided in Appendix 1. Amplification and Sequencing— Two loci were amplified and there are several additional genera with fruits similar to those sequenced; trnL-F (primers F and C, Taberlet et al. 1991) from the chloro- of Thysanocarpus in the tribes Alysseae, Heliophileae, and plast genome and the nuclear ribosomal ITS (primers ITS5 and ITS4, White Isatideae. The similarity of Thysanocarpus to Tauscheria Fisch. et al. 1990). Amplification and sequencing followed previously developed (currently included in Isatis L.) in particular was noted by protocols ( Bailey and Doyle 1999 ; Bailey et al. 2002 ), and both loci were successfully amplified and sequenced for all samples except trnL-F for Hooker (1829) , Torrey and Gray (1838–40), and Greene (1891). one accession of T. desertorum (32) and ITS for one T. curvipes (26) and one However, recent molecular phylogenetic investigations sug- T. erectus (38). Most sequences were generated by direct sequencing of PCR gest that these taxaProof with similar fruits are not closely related products.Only However, initial direct sequencing attempts for ITS products in 1 2 SYSTEMATIC BOTANY [Volume 35 Thelypodieae. The sequence data for T. laciniatus includes conflict between the two loci caused by hybridization (see Discussion). Consequently, application of cladistic methodology to a concatenated dataset including trnL-F and ITS sequences for T. laciniatus is inappropriate, because the resulting terminals would violate a fundamental assumption of cladistic analysis, that character state change occurs along a common bifurcat- ing evolutionary history ( Bremer and Wanntorp 1979 , Brower et al. 1996 , Proof CronquistOnly 1987 ). Matrix 1 was rooted with Aethionema grandiflorum Boiss. & Hohen., a member of the genus that is well-supported as sister to all other extant Brassicaceae ( Al-Shehbaz et al. 2006 ; Bailey et al. 2006 ). Matrices 2, 3, and 4 are used to investigate relationships within Thysanocarpus . Matrix 2 contains ITS sequences for all Thysanocarpus samples, including multiple sequences from accessions of T. laciniatus as described above. Matrix 3 contains trnL-F sequences for all Thysanocarpus samples. Matrix 4 is a concatenated data set containing both ITS and trnL- F samples for all Thysanocarpus except T. laciniatus . The single accession (26) of T. curvipes for which only a trnL-F sequence was available was also excluded from Matrix 4. Phylogenetic relationships among members of Thelypodieae are insufficiently resolved to identify the sister group of Thysanocarpus ( Bailey et al. 2006 ; and see Results). To root our analyses, we chose Streptanthella longirostris (S. Wats.) Rydb., a member of Thelypodieae that is resolved in a large polytomy with Thysanocarpus . However, iden- tical interspecific relationships were recovered in analyses including all sampled members of Thelypodieae (Matrix 1; Fig. 3 ; see Results) suggest- F3 ing that outgroup selection has not affected inferred relationships within Thysanocarpus . Matrices were aligned automatically using ClustalW ( Thompson et al. 1994 ) under default parameters. The resulting alignments were then checked and refined manually
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