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Multigene Approaches to the Phylogeny of Amaryllidaceae

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Multigene Approaches to the Phylogeny of Amaryllidaceae Aliso 22, pp. 355–366 ᭧ 2006, Rancho Santa Ana Botanic Garden THE NEVER-ENDING STORY: MULTIGENE APPROACHES TO THE PHYLOGENY OF AMARYLLIDACEAE ALAN W. M EEROW1,3 AND DEIRDRE A. SNIJMAN2 1USDA-ARS-SHRS, National Germplasm Repository, 13601 Old Cutler Road, Miami, Florida 33158, USA; 2Compton Herbarium, South African National Biodiversity Institute, Kirstenbosch, Rhodes Drive, Newlands, Cape Town, South Africa 3Corresponding author ([email protected]) ABSTRACT Results to date with various plastid genes confirmed the monophyly of the Amaryllidaceae s.s. as a whole, strongly supported the mostly African tribe Amaryllideae as sister to the rest of the family, and resolved geographically-based monophyletic groups, but failed to resolve the relationships among several basal lineages in the family (the African Haemantheae and Cyrtantheae, the Australasian Calostemmateae, and the American and Eurasian sister clades). We present analysis of plastid ndhF sequences that fully resolved the major clades of the family. The baccate-fruited Haemantheae and Calostemmateae are sister tribes, and the African endemic Cyrtantheae is sister to them both. This clade is sister to an American/Eurasian clade. We also present preliminary nuclear ribosomal ITS sequence analysis of the Eurasian clade. Lycorideae are basal in the group and begin a grade that continues with Hannonia, then Pancratium, then Lapiedra. The genera Galanthus, Narcissus, and Sternbergia are resolved as monophyletic with strong support. Leucojum is paraphyletic and recog- nition of Acis for the mostly autumn-flowering Mediterranean species is supported. Recent phyloge- netic analyses of various tribes and genera of the family are reviewed. Above the family level, Aga- panthaceae, Alliaceae, and Amaryllidaceae form a well-supported monophyletic group, but exact res- olution of the relationships among the three subclades varies depending on the sequence matrix uti- lized. The Angiosperm Phylogeny Group II has advocated combining all three into a single family, Alliaceae. We discuss this decision, which has historical precedent, but recommend that Amaryllida- ceae be conserved as the name for the family in such a treatment. Key words: Amaryllidaceae, Asparagales, cladistics, DNA, monocotyledons, phylogeny. INTRODUCTION (among them Calostemmateae) and 19 subtribes, many of Amaryllidaceae are one of the few families of the higher them monogeneric; Meerow and Snijman (1998) recognized Asparagales well defined by other than molecular characters, 13 tribes, with two subtribes only in one of them. Discussion namely the combination of umbellate cymes, inferior ova- of character evolution within the family can be found in ries, and unique alkaloid chemistry (Meerow and Snijman Meerow (1995), Meerow and Snijman (1998), and Meerow 1998), but morphological characters alone fail to adequately et al. (1999). resolve phylogenetic relationships within the family (Mee- The precise relationship of Amaryllidaceae to other As- row et al. 2000a). Some of these characters, such as inflo- paragales remained elusive until Fay and Chase (1996) used rescence type, are likely synapomorphies for a deeper group- molecular data to argue that Agapanthaceae, Alliaceae, and ing of families (Agapanthaceae, Alliaceae) that could be sub- Amaryllidaceae form a monophyletic group (also evident in sumed in Amaryllidaceae (though this name would need to Chase et al. 1995) and that together they are related most be conserved over Alliaceae). The four most recent infra- closely to Hyacinthaceae s.s. and the resurrected family familial classifications of Amaryllidaceae are those of Traub Themidaceae (the former tribe Brodiaeeae of Alliaceae). (1963), Dahlgren et al. (1985), Mu¨ller-Doblies and Mu¨ller- They recircumscribed Amaryllidaceae to include Agapan- Doblies (1996), and Meerow and Snijman (1998). Traub’s thus L’He´r., previously included in Alliaceae, as subfamily scheme included Alliaceae, Hemerocallidaceae, and Ixioli- Agapanthoideae. This recircumscription was based on phy- riaceae as subfamilies, in part following Hutchinson (1934, logenetic analysis of plastid rbcL sequence data, with only 1959). Within his subfamily Amaryllidoideae, he erected four genera of Amaryllidaceae s.s. included in the analysis. two informal taxa, ‘‘infrafamilies’’ Amarylloidinae and Pan- All the epigynous genera were treated as Amaryllidoideae. cratioidinae, both of which were polyphyletic (Meerow Subsequent analyses of multiple DNA sequences from both 1995). Dahlgren et al. (1985) dispensed with any subfamilial the chloroplast and nuclear genomes have shown quite classification above the level of tribe, recognizing eight, and strongly that Agapanthus, Amaryllidaceae, and Alliaceae treated as Amaryllidaceae only those genera in Traub’s represent a distinct lineage within the monocot order Aspar- Amaryllidoideae. Stenomesseae and Eustephieae were com- agales (Meerow et al. 1999; Fay et al. 2000), but the exact bined. Meerow (1995) resurrected Eustephieae from Steno- relationships among the three groups have been difficult to messeae and suggested that two new tribes might need to be resolve with finality (Graham et al. 2006). recognized, Calostemmateae and Hymenocallideae. Mu¨ller- Meerow et al. (1999) presented cladistic analyses of plas- Doblies and Mu¨ller-Doblies (1996) recognized ten tribes tid DNA sequences rbcL and trnL–F alone and in combi- 356 Meerow and Snijman ALISO nation for 51 genera of Amaryllidaceae and 31 genera of with a bootstrap ϭ 93%. In both of the major American related asparagalean families. The combined analysis was clades, there is a small tribe that is sister to the rest of the the most highly resolved of the three and provided good clade, Eustephieae in the Andean group, and Griffineae in support for the monophyly of Amaryllidaceae and indicated the hippeastroid clade. These two small tribes may represent Agapanthaceae as its sister family (though bootstrap support either ancestral or merely very isolated elements of their for this relationship was still weak at 60%). Alliaceae were respective clades. in turn sister to the Amaryllidaceae/Agapathaceae clade. In To date, the relationships of the remaining endemic Af- Fay et al.’s (2000) analysis of Asparagales using four chlo- rican tribal clades of the family after Amaryllideae branches roplast DNA regions, Alliaceae were resolved as sister to remain unresolved. In the intervening years since Monocots Amaryllidaceae, with Agapanthus sister to them both. Again, II in Sydney (Wilson and Morrison 2000), we have been bootstrap support was weak at best. Based on these data, it working on several fronts. A number of generic and tribal would be possible to argue for recognizing Amaryllidaceae phylogenetic analyses have been completed (Meerow and in a modified Hutchinsonian (1934) sense, i.e., with three Snijman 2001; Meerow et al. 2002, 2003; Meerow and Clay- subfamilies, Agapanthoideae, Allioideae, and Amarylli- ton 2004). In this paper we review the progress made on doideae. Meerow et al. (1999) opted to recognize a mono- amaryllid phylogeny since Monocots II and present the first typic Agapanthaceae. The latest Angiosperm Phylogeny results of phylogenetic analyses across the entire family us- Group (AGP II 2003) recommends treating all three as a ing plastid ndhF sequences, as well as preliminary analyses single family, Alliaceae (which currently has nomenclatural of the Eurasian clade of the family using ITS. priority), but also optionally suggest recognition of ‘‘Amar- yllidaceae s.s.’’ using their ‘‘bracketing’’ system. MATERIALS AND METHODS Based on the cladistic relationships of chloroplast DNA sequences (Meerow et al. 1999) the family originated in Af- Sampling rica and infrafamilial relationships are resolved along bio- Genomic DNA was extracted from silica gel dried leaf geographic lines. Tribe Amaryllideae, entirely southern Af- tissue of the taxa listed in Table 1 as described by Meerow rican with the exception of pantropical Crinum L., were sis- et al. (2000b). GenBank accession numbers are listed in Ta- ter to the rest of Amaryllidaceae with very high bootstrap ble 1. support. The remaining two African tribes of the family, Haemantheae (including Gethyllideae) and Cyrtantheae, DNA Extraction, Amplification, and Sequencing Protocols were well supported, but their position relative to the Aus- tralasian Calostemmateae and a large clade comprising the Amplification of the ribosomal DNA ITS1/5.8S/ITS2 re- Eurasian and American genera, was not clear. Most surpris- gion was accomplished using flanking primers (in the 18S ing, the Eurasian and American elements of the family were and 26S loci) AB101 and AB102 (Douzery et al. 1999) and each monophyletic sister clades. Ito et al. (1999) resolved a the original White et al. (1990) internal primers ITS2 and very similar topology for a more limited sampling of Amar- ITS3 were used to amplify the spacers along with the inter- yllidaceae and related asparagoids using plastid matK se- vening 5.8S gene as described by Meerow et al. (2000b). quences, but Agapanthus was sister to a diverse clade of The plastid ndhF gene was amplified and sequenced using Agavaceae, Anthericaceae, Funkiaceae, and Hyacinthaceae the eight primers of Olmstead and Sweere (1994). All poly- in their trees, the former three families represented by a sin- merase chain reaction (PCR) amplifications were performed gle species each. There was no bootstrap support for this on a Gene Amp௡ PCR System 9700 (Perkin-Elmer Applied position of Agapanthus in their
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