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(Tribe Haemantheae) Inferred from Plastid and Nuclear Non-Coding DNA Sequences

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(Tribe Haemantheae) Inferred from Plastid and Nuclear Non-Coding DNA Sequences Plant Syst. Evol. 244: 141–155 (2004) DOI 10.1007/s00606-003-0085-z Generic relationships among the baccate-fruited Amaryllidaceae (tribe Haemantheae) inferred from plastid and nuclear non-coding DNA sequences A. W. Meerow1, 2 and J. R. Clayton1 1 USDA-ARS-SHRS, National Germplasm Repository, Miami, Florida, USA 2 Fairchild Tropical Garden, Miami, Florida, USA Received October 22, 2002; accepted September 3, 2003 Published online: February 12, 2004 Ó Springer-Verlag 2004 Abstract. Using sequences from the plastid trnL-F Key words: Amaryllidaceae, Haemantheae, geo- region and nrDNA ITS, we investigated the phy- phytes, South Africa, monocotyledons, DNA, logeny of the fleshy-fruited African tribe Haeman- phylogenetics, systematics. theae of the Amaryllidaceae across 19 species representing all genera of the tribe. ITS and a Baccate fruits have evolved only once in the combined matrix produce the most resolute and Amaryllidaceae (Meerow et al. 1999), and well-supported tree with parsimony analysis. Two solely in Africa, but the genera possessing main clades are resolved, one comprising the them have not always been recognized as a monophyletic rhizomatous genera Clivia and Cryp- monophyletic group. Haemanthus L. and tostephanus, and a larger clade that unites Haemanthus and Scadoxus as sister genera to an Gethyllis L. were the first two genera of the Apodolirion/Gethyllis subclade. One of four group to be described (Linneaus 1753). Her- included Gethyllis species, G. lanuginosa, resolves bert (1837) placed Haemanthus (including as sister to Apodolirion with ITS. Relationships Scadoxus Raf.) and Clivia Lindl. in the tribe among the Clivia species are not in agreement with Amaryllidiformes, while Gethyllis was classi- a previous published phylogeny. Biogeographic fied with Sternbergia L. in Oporanthiformes. analysis using the divergence/vicariance method Salisbury (1866) recognized the distinct tribes roots the tribe in Eastern South Africa, with several Haemantheae Salisb. and Gethyllideae Salisb. subsequent dispersals to the winter rainfall Western Bentham and Hooker (1883) united Crypto- Cape region. Chromosomal change from an ances- stephanus Baker with Narcissus L. in their tral 2n ¼ 22 (characteristic of Clivia) is associated subtribe Coronatae, while maintaining with each main clade. Reduction in number has Haemanthus, Clivia Lindl. and Apodolirion occurred in all but Cryptostephanus, which has Baker in subtribe Genuinae. Cryptostephanus 2n ¼ 24 chromosomes. Increasing the sampling across all of the species in the tribe will allow a has perianthal appendages at the throat of the more detailed understanding of the biogeographic flower that Bentham and Hooker (1883) patterns inherent in the parsimony topology, which considered homologous to the corona of undoubtedly reflect Quaternary climatic changes in Narcissus. Pax (Pax 1887) situated Haeman- Southern Africa. thus and Clivia in his subtribe Haemanthinae 142 A. W. Meerow and J. R. Clayton: Molecular systematics of Haemantheae Pax, placed Gethyllis and Apodolirion in that study beyond the well-supported sister Zephyranthinae (on the basis of their fused relationship of Apodolirion and Gethyllis which spathe bracts and single-flowered inflorescenc- together terminated a successive grade begin- es), and Cryptostephanus within Narcissinae, a ning with Clivia, followed by Cryptostephanus, treatment largely followed by Hutchinson Scadoxus and Haemanthus. However, boot- (1934), though Pax’s (1887) subtribes were strap support for each branch in the grade was elevated to the rank of tribe. All of these moderate to strong. Ito et al. (1999), using groups were polyphyletic, uniting genera from plastid matK sequences also resolved a mono- disparate lineages within the family (see dis- phyletic Haemantheae, though only three gen- cussion by Nordal and Duncan 1984). era were sampled. Haemanthus and Scadoxus Traub (1963) was the first to recognize the were sister taxa in their study with 98% relationship between Clivia and Cryptosteph- bootstrap support. anus, but placed both as the sole genera in tribe As treated here, Haemantheae consists of Clivieae Traub. Haemanthus was relegated to six genera. Cryptostephanus (2 spp.) and Clivia the monotypic Haemantheae, while Gethyllis (5 spp.) are bulbless, rhizomatous perennials. and Apodolirion were placed alone in Gethylli- With the exception of the newly described deae, with the suggestion that the two genera Clivia mirabilis Rourke, both genera are found were likely indistinct. Melchior (1964) placed in summer rainfall regions. Clivia is adapted to both Clivia and Cryptostephanus in Haeman- butterfly and sunbird pollination, and has theae. Dahlgren et al. (1985) largely adopted showy orange and yellow flowers. The species Traub’s (1963) classification, though Gethylli- are chiefly understory herbs of coastal and deae and Clivieae were subsumed in Haeman- Afro-montane forest. The two species of theae. Cryptostephanus are either savanna or forest The two most recent formal classifications herbs. The small flowers have a paraperigone, of the Amaryllidaceae are those of Mu¨ller- and it is the only genus in the tribe whose seeds Doblies and Mu¨ller-Doblies (1996), and Mee- have a phytomelanous testa. Scadoxus (9–12 row and Snijman (1998). Both recognized two spp.) and Haemanthus (21 spp.) have long been tribes for the baccate-fruited genera: Haeman- recognized intuitively as sister taxa (in the past theae (Haemanthus, Scadoxus, Clivia and treated as a single genus; e.g. Bjo¨rnstad and Cryptostephanus) and Gethyllideae (Gethyllis Friis 1972). Both genera have brush-like inflo- and Apodolirion). Mu¨ller-Doblies and Mu¨ller- rescence morphology, in which the bracts often Doblies (1996) further recognized two sub- form part of the pollinator attraction system. tribes in Haemantheae, Haemanthinae D. & Scadoxus are forest understory herbs, some U.M.-D. (Haemanthus and Scadoxus) and species of which do not form true bulbs. The Cliviinae D. & U.M.-D. (Clivia and Crypto- genus is most common in the African tropics. stephanus). Scadoxus was segregated from Haemanthus, all species forming bulbs, is Haemanthus by Friis and Nordal (1976). All strictly southern African, with species in both of the baccate-fruited genera are endemic to the summer and winter rainfall regions of the Africa. Cape (Snijman 1984). Finally, Gethyllis (ca. 35 Meerow et al. (1999), using three plastid species, Mu¨ller-Doblies 1986) and Apodolirion DNA sequences, confirmed the monophyly of (ca. 6 species, Mu¨ller-Doblies 1986) are two Haemantheae, but indicated that Gethyllideae closely related uni-flowered Cape endemics was embedded within the former tribe, and that both retain the ovary inside the bulbs thus could not be recognized without render- until the large, fleshy, aromatic fruit matures. ing Haemantheae paraphyletic. The level of They are differentiated by the capitate stigma sampling and the number of phylogenetically in Gethyllis (vs. tri-lobed in Apodolirion) and informative base substitutions were insufficient the often numerous stamens in Gethyllis (vs. to resolve the relationships within the tribe in six in Apodolirion). Gethyllis is most common A. W. Meerow and J. R. Clayton: Molecular systematics of Haemantheae 143 in the winter rainfall region of South Africa, The plastid trnL-F matrix consisted of the same 19 Apodolirion in the summer rainfall zone. taxa, plus the addition of Haemanthus humilis. The purpose of this present study was to Amaryllis is the basal most genus within the tribe establish baseline generic relationships of the Amaryllideae (Meerow and Snijman 2001) that in genera of the Haemantheae by increasing the turn is sister to the rest of the Amaryllidaceae. The sampling for the plastid trnL-F region, and sister group relationships of Haemantheae are so far unresolved (Meerow et al. 1999). We experi- adding sequences from the internally tran- mented with a species of Cyrtanthus Herb. scribed spacer (ITS) of nuclear ribosomal (Cyrtantheae) and Calostemma R. Brown DNA. (Calostemmateae) as outgroups, but found that Amaryllis presented the least number of alignment Materials and methods ambiguities and generated the shortest trees. Res- olution of the sister relationships of Haemantheae Sampling. Genomic DNA was extracted from remain unclear (Meerow et al. 1999); however the silica gel dried leaf tissue of the taxa listed in tribe Amaryllideae is sister to all other genera in the Table 1 as described by Meerow et al. (2000). family with high bootstrap support, even with as DNA extraction, amplification and sequencing highly conserved a gene as rbcL (Meerow et al. protocols. The trnL-trnF region was amplified and 1999). At present we are working to successfully sequenced using the primers of Taberlet et al. align ITS sequences across the entire Amaryllida- (1991) as described by Meerow et al. (1999). ceae in order to resolve the basal polytomy that Amplification of the ribosomal DNA ITS1/5.8S/ resolves after the branching of tribe Amaryllideae ITS2 region was accomplished using flanking with all plastid sequences that have been applied to primers (18S, 26S) AB101 and AB102 (Douzery the problem to date (Ito et al. 1999; Meerow et al. et al. 1999), and the original White et al. (1990) 1999, 2000). We feel it is better to use as outgroup internal primers ITS2 and 3 to amplify the spacers the most basal genus in a tribe that is indisputably along with the intervening 5.8S intron as described outside of the ingroup of interest. by Meerow et al. (2000). All polymerase chain Aligned
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