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Systematics of Bromelioideae (Bromeliaceae)—Evidence from Molecular and Anatomical Studies Ralf Horres J.W

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Systematics of Bromelioideae (Bromeliaceae)—Evidence from Molecular and Anatomical Studies Ralf Horres J.W Aliso: A Journal of Systematic and Evolutionary Botany Volume 23 | Issue 1 Article 5 2007 Systematics of Bromelioideae (Bromeliaceae)—Evidence from Molecular and Anatomical Studies Ralf Horres J.W. Goethe-Universität & Forschungsinstitut Senckenberg, Frankfurt am Main, Germany Katharina Schulte J.W. Goethe-Universität & Forschungsinstitut Senckenberg, Frankfurt am Main, Germany Kurt Weising Universität Kassel, Germany Georg Zizka J.W. Goethe-Universität & Forschungsinstitut Senckenberg, Frankfurt am Main, Germany Follow this and additional works at: http://scholarship.claremont.edu/aliso Part of the Botany Commons, and the Ecology and Evolutionary Biology Commons Recommended Citation Horres, Ralf; Schulte, Katharina; Weising, Kurt; and Zizka, Georg (2007) "Systematics of Bromelioideae (Bromeliaceae)—Evidence from Molecular and Anatomical Studies," Aliso: A Journal of Systematic and Evolutionary Botany: Vol. 23: Iss. 1, Article 5. Available at: http://scholarship.claremont.edu/aliso/vol23/iss1/5 Aliso 23, pp. 27–43 ᭧ 2007, Rancho Santa Ana Botanic Garden SYSTEMATICS OF BROMELIOIDEAE (BROMELIACEAE)—EVIDENCE FROM MOLECULAR AND ANATOMICAL STUDIES RALF HORRES,1,3,4 KATHARINA SCHULTE,1 KURT WEISING,2 AND GEORG ZIZKA1 1Department of Botany and Molecular Evolution, J. W. Goethe-Universita¨t and Forschungsinstitut Senckenberg, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany ([email protected]), ([email protected]); 2Systematik und Morphologie der Pflanzen, Fachbereich Naturwissenschaften, Universita¨t Kassel, D-34109 Kassel, Germany ([email protected]) 3Corresponding author ([email protected]) ABSTRACT A reconstruction of the phylogeny of Bromeliaceae based on sequence data from three noncoding chloroplast DNA markers (trnL intron, trnT–trnL, and trnT–trnF intergenic spacer [IGS]) is presented, including 26 genera and 33 species. Relationships of Bromelioideae and phylogeny within this sub- family were analyzed in more detail on the basis of two of these markers (trnL intron and trnL–trnF IGS) using a set of 37 genera/74 species of Bromeliaceae, including 28 genera/60 species of Bro- melioideae. Sister group relationships of Bromelioideae were not resolved with sufficient reliability, but the most likely candidates are the genera Fosterella and Puya. The basal phylogeny of Brome- lioideae also was not resolved. Greigia, Ochagavia/Fascicularia/Fernseea, Deinacanthon, Bromelia, and a ‘‘core group’’ of the remaining Bromelioideae formed a basal polytomy. Within Bromelioideae, the AFLP technique was applied to assess relationships among selected groups of genera. In the Ochagavia/Fascicularia group (5 species and subspecies/16 accessions), AFLP data fully confirmed the systematic relationships based on morphological and anatomical characters. Investigation of 30 Aechmea species (33 accessions), including all subgenera and one species each from the related genera Ursulaea, Portea, Chevaliera, and Streptocalyx produced no resolution for several of the species. Clades that received good bootstrap support generally did not correspond with the delimitation of subgenera of Aechmea. Additionally, leaf blade anatomy of these species was investigated. The results corresponded partly with those of the AFLP analysis. Generic rank for Ursulaea and Portea was not supported. Key words: Aechmea, AFLPs, Bromeliaceae, Fascicularia, Greigia, Ochagavia, phylogeny, trnL in- tron, trnL–trnF, trnT–trnL IGS. INTRODUCTION Aechmea have become clear, but still there is no convincing and commonly accepted concept for (sub)generic delimita- Bromeliaceae is a medium-sized family comprising 56 tion in most groups. Molecular data are expected to provide genera with more than 2600 species (Smith and Till 1998). the most valuable information in this respect, but of equal The almost exclusively Neotropical bromeliads have been importance is further research on morphology and anatomy very successful as colonizers of epiphytic as well as terres- and the variability of relevant characters within bromeliads. trial habitats. Unique trichomes capable of water absorption Several molecular studies have dealt with the phylogeny and the development of various strategies to deal with water of the family (see Table 1) and provided important new in- stress (succulence, foliar impoundment, CAM photosynthe- sights. Nevertheless, most of these studies suffered from lim- sis) allow an extraordinary ecological versatility in the fam- ited taxon sampling and from the fact that they were often ily. In spite of the species richness of bromeliads, their abun- based on single markers, usually of the chloroplast genome. dance in many Neotropical habitats, and their importance as Another weakness is the unusually low sequence variability ornamentals, updated revisions are lacking for most of the of all markers investigated in Bromeliaceae so far, leading genera, especially for the most species-rich ones. to low phylogenetic resolution, especially in the subfamilies Different generic concepts have been proposed resulting Tillandsioideae and Bromelioideae. in many new combinations, usually without being based on The monophyly of Bromeliaceae, which was commonly new revisional work. The elevation of the eight subgenera accepted on the basis of morphological and anatomical fea- of Aechmea Ruiz & Pav. (Bromelioideae) to generic rank by tures before (e.g., unique epidermal trichomes, flower mor- Smith and Kress (1989, 1990), as well as the sinking of phology, silica bodies of epidermal cells, as in Dahlgren et Streptocalyx Beer in Aechmea proposed by Smith and Spen- al. 1985), has been confirmed by all molecular studies. cer in 1992 was rigorously criticized by Brown et al. (1993), While in Angiosperm Phylogeny Group (APG) 1998, Bro- as it was not accompanied by a thorough reevaluation of the meliaceae are placed within a commelinoid clade without affected taxa. identifying their sister group and closer relationships, the The weaknesses of the delimitations of genera such as later phylogenies proposed by Chase et al. (2000) and APG II (2003) reveal the family as part of the order Poales. 4Present address: Head of Marker Technologies, GenXPro GmbH, Among this order, Rapateaceae is sister to a clade with all FIZ, Altenho¨ferallee 3, D-60438 Frankfurt am Main, Germany. the other families, including Bromeliaceae. The latter is sis- 28 Horres, Schulte, Weising, and Zizka ALISO Table 1. Recently published studies on the phylogeny of Bromeliaceae based on molecular data. T: Tillandsioideae, B: Bromelioideae, P: Pitcairnioideae (sensu Smith and Till 1998). Molecular Data Authors Marker Genera/species of Bromeliaceae Ranker et al. (1990) restriction sites (cp) 9/10 (T: 4/5, P: 3/3, B: 2/2) Givnish et al. (1990) restriction sites (cp) 7/7 Clark and Clegg (1990) rbcL 3/3 Clark et al. (1993) rbcL 7/7 Duvall et al. (1993) rbcL 7/7 (T: 3/3, P: 2/2, B: 2/2) Terry and Brown (1996) ndhF 30/51 (T: 7/28, P: 8/8, B: 15/15) Givnish et al. (1997) restriction sites (nr ϩ cp) 4/19 (mostly Brocchinia; P: 4/19) Terry et al. (1997a) ndhF 29/30 (T: 6/7, P: 8/8, B: 15/15) Terry et al. (1997b) ndhF 9/28 (mostly Tillandsioideae) Horres et al. (2000) trnL intron 32/62 (T: 7/23, P: 9/19, B: 16/20) Behnke et al. (2000) rbcL 11/11 (T: 2/2, P: 5/5, B: 4/4) Crayn et al. (2000) matK 15/40 (mostly Pitcairnioideae; T: 3/3, P: 11/36, B: 1/1) Reinert et al. (2003) matK 11/35 (analysis of data by Crayn et al. 2000, P: 11/35) Crayn et al. (2004) matK&rps16 intron 24/51 (T: 7/10, P: 9/33, B: 8/8) Givnish et al. (2005) ndhF 25/35 (T: 5/5, P: 14/24, B: 6/6) ter to a branch with Poaceae, Anarthriaceae, Restionaceae, terocohnia Mez/Dyckia Schult. f./Encholirium Mart. ex Flagellariaceae, Xyridaceae, Cyperaceae, Juncaceae, Thur- Schult., Fosterella, and Navia igneosicola L. B. Sm., Stey- niaceae, and Mayacaceae (Chase et al. 2000). In a study of erm. & H. Rob., occurs on a clade with the majority of ndhF cpDNA data analysis, Givnish et al. (2006) found that Pitcairnia L’He´r. species (‘‘Pitcairnia 2’’), while P. burle- members of Typhaceae are sister to Bromeliaceae at the base marxii Braga & Sucre, P. carinata Mez, and P. heterophylla of the order Poales sensu APG II (2003), with Rapateaceae (‘‘Pitcairnia 1’’) are well supported on a separate clade, and next divergent. Puya is sister to Bromelioideae (68% bootstrap support). Our molecular studies of the trnL intron alone (Horres et Based on the analysis of ndhF data by Givnish et al. al. 2000) revealed a clade comprising Brocchinia Schult. & (2006; see Table 1) the monophyly of Tillandsioideae is sup- Schult. f. and Ayensua L. B. Sm. as sister to the remainder ported with 57% bootstrap support only. The matK and of the family. Among the latter, three principal branches can rps16 intron data by Crain et al. (2004) support this finding be discerned: one lineage comprising the members of Til- with bootstrap values of 85%. Although all of these studies landsioideae; a second formed by the representatives of provide new insights, especially for Pitcairnioideae, there re- Hechtia; and a third containing all Bromelioideae and the main partly conflicting topologies so that phylogeny within remaining Pitcairnioideae (except Brocchinia, Ayensua, and Bromeliaceae is far from clear. Pitcairnioideae was the only Hechtia Klotzsch). In this third lineage, Bromelioideae are subfamily that had been grouped into tribes (Brocchineae, monophyletic, but the phylogeny of Puya Molina, Fosterella Puyeae, and Pitcairnieae), based on the studies of Varada- L. B. Sm., and the other Pitcairnioideae is not resolved. rajan and Gilmartin (1988a, b; see also Smith and Till 1998). These results correspond with those obtained from the ndhF The molecular data at hand contradict such a systematic con- gene by Terry et al. (1997a) as far as the basal position of cept by showing that the subfamily in its traditional circum- Brocchinia is concerned (Ayensua was not studied by these scription is paraphyletic (Givnish et al. 1997, 2006; Terry et authors). However, the ndhF tree differs in identifying Puya al. 1997a; Crayn et al. 2000, 2004; Horres et al. 2000). as sister to Bromelioideae and Fosterella as part of a clade Monophyly for Tillandsioideae has been confirmed by all of Pitcairnioideae s.s.
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