View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector South African Journal of Botany 2004, 70(3): 371–381 Copyright © NISC Pty Ltd Printed in South Africa — All rights reserved SOUTH AFRICAN JOURNAL OF BOTANY ISSN 0254–6299 Recent advances in understanding Apiales and a revised classification GM Plunkett1*, GT Chandler1,2, PP Lowry II3, SM Pinney1 and TS Sprenkle1 1 Department of Biology, Virginia Commonwealth University, PO Box 842012, Richmond, Virginia 23284-2012, United States of America 2 Present address: Department of Biology, University of North Carolina, Wilmington, North Carolina 28403-5915, United States of America 3 Missouri Botanical Garden, PO Box 299, St Louis, Missouri 63166-0299, United States of America; Département de Systématique et Evolution, Muséum National d’Histoire Naturelle, Case Postale 39, 57 rue Cuvier, 75231 Paris CEDEX 05, France * Corresponding author, e-mail: [email protected] Received 23 August 2003, accepted in revised form 18 November 2003 Despite the long history of recognising the angiosperm Apiales, which includes a core group of four families order Apiales as a natural alliance, the circumscription (Apiaceae, Araliaceae, Myodocarpaceae, Pittosporaceae) of the order and the relationships among its constituent to which three small families are also added groups have been troublesome. Recent studies, howev- (Griseliniaceae, Torricelliaceae and Pennantiaceae). After er, have made great progress in understanding phylo- a brief review of recent advances in each of the major genetic relationships in Apiales. Although much of this groups, a revised classification of the order is present- recent work has been based on molecular data, the ed, which includes the recognition of the new suborder results are congruent with other sources of data, includ- Apiineae (comprising the four core families) and two ing morphology and geography. A unified picture of rela- new subfamilies within Apiaceae (Azorelloideae and tionships has now emerged regarding the delimitation of Mackinlayoideae). Introduction Almost all authors have considered the dicot families made in the ordinal classification of Apiales (Dahlgren 1980 Apiaceae and Araliaceae closely related (e.g. Bentham and being the only notable exception). In the past ten years, Hooker 1867, Engler and Prantl 1898, Bessey 1915, however, a unified picture of relationships has rapidly Dahlgren 1980, Cronquist 1981, 1988, Takhtajan 1987, emerged regarding both the circumscription and internal Thorne 1992, but see Hutchinson 1967, 1973) and have relationships of the order. Similar progress has been made usually treated them in the same order, albeit under various in many other angiosperm orders, and several ongoing names, including Umbellales, Cornales (when associated efforts are now underway to formalise the results of these with Cornaceae), Araliales, and Apiales (the name we shall advances (APG 1998, 2003, Stevens 2003). Most authors use hereafter). The near-ubiquity of this interpretation stands working on Apiales have hesitated to provide a formal recir- in stark contrast to the diverse treatments both above and cumscription of the order during this ‘period of discovery’. below the ordinal level, such as the placement of Apiales The recent publication of a new apialean classification by an among the other orders of dicots, the inclusion of additional author with little or no expertise in the group (Doweld 2001), families within the order (Cornaceae, Torricelliaceae, including the description of two new families based on our Helwingiaceae, Griseliniaceae, etc.), and the many inter- own work (viz. Plunkett and Lowry 2001), has prompted us and infrafamilial treatments of Apiaceae and Araliaceae to provide both a formal classification of Apiales together themselves. As with many higher taxonomic groups, the dif- with a review of the relevant literature upon which our deci- ficulties in sorting out relationships in Apiales presumably sions are based. We hope this effort will also provide a fitting stem from repeated cycles of divergence and migration, fol- framework from which the other contributions to this sympo- lowed by convergence and parallelism. sium volume can be better understood. In the decades immediately preceding the development of Several publications already provide comprehensive objective approaches to phylogenetic analysis (e.g. parsi- reviews of the taxonomic history of Apiales and/or their con- mony, phenetic, and likelihood methods) and the use of stituent groups (e.g. Constance 1971, Heywood 1978, molecular sources of data, few substantial advances were Plunkett et al. 1996a, 1996b, 1997, Downie et al. 2001, 372 Plunkett, Chandler, Lowry, Pinney and Sprenkle Plunkett and Lowry 2001, Plunkett 2001), and therefore this step that we now take with the description of Azorelloideae information is not repeated herein. Instead, we focus on as a new subfamily of Apiaceae in Table 1. reviewing (or in some cases previewing) results from recent A third group of ‘hydrocotyloids’ forms a clade together studies (or unpublished work) completed since the publica- with two genera traditionally referred to Araliaceae, tion of the preceding Apiales Special Issue of the Edinburgh Mackinlaya and Apiopetalum. This clade is currently recog- Journal of Botany (2001, Volume 58, no. 2). Following this, nised either as a tribe (Mackinlayeae, e.g. in Plunkett and we provide a formal recircumscription and interfamilial clas- Lowry 2001), a family (Mackinlayaceae, Doweld 2001), or sification of the order. simply as the ‘Mackinlaya group’ (Chandler and Plunkett 2004). In addition to Mackinlaya and Apiopetalum, it Apiaceae includes the ‘hydrocotyloid’ genera Centella, Micropleura, Actinotus, Platysace, Xanthosia and possibly other, as yet In their contributions to the last symposium volume, both unsampled, genera (see Plunkett et al. 1997, Downie et al. Plunkett (2001) and Downie et al. (2001) explored relation- 2000, Plunkett and Lowry 2001, Chandler and Plunkett ships within Apiaceae using ‘supertree’ and ‘consensus’ 2004). In the study of Chandler and Plunkett (2004), a approaches, respectively (Downie et al. 2001 also examined Bayesian inference tree based on combined 26S rDNA, relationships within subfamily Apioideae using a ‘combined rbcL, and matK data place the Mackinlaya group as sister to data’ approach). With the exception of Chandler and core Apiaceae (Figure 1), in agreement with an earlier study Plunkett (2004), most recent studies of Apiaceae have using matK and ITS rDNA data (Plunkett and Lowry 2001). focused on relationships within subfamilies and/or among These results are supported by several morphological char- genera (e.g. Lee et al. 2001, Spalik et al. 2001a, 2001b, acters that serve to link the Mackinlaya group to Apiaceae, Valiejo-Roman et al. 2002, Liu et al. 2003), and relatively few such as laterally-compressed bicarpellate fruits, valvate developments have been made in the familial and subfamil- petals that are both clawed and inflexed, and sheathing peti- ial classification of Apiaceae during the past two years. ole bases. For this reason, we recognise the Mackinlaya Unfortunately, several different definitions of Apiaceae are group as a distinct subfamily of Apiaceae, which is likewise currently in use, including the traditional circumscription formally published as Mackinlayoideae in Table 1. (Drude 1898 as updated by Pimenov and Leonov 1993), a Great progress has recently been made in re-circumscrib- much more expansive circumscription that includes both ing subfamily Saniculoideae. In their study of fruit structure, Apiaceae (sensu Drude) and Araliaceae (e.g. Judd et al. Liu et al. (2003) refined the list of carpological features that 2002), and a narrower concept generally referred to as ‘core characterise Saniculoideae, which now includes (with some Apiaceae’ (originally coined by Plunkett et al. 1997). Core exceptions) the presence of non-lignified endocarps, meri- Apiaceae are in large part consistent with Drude’s familial carp outgrowths, and prominent intrajugal secretory ducts and subfamilial concepts, but not his tribes, which rarely cor- (also called ‘companion canals’ by Tseng 1967), plus the respond to monophyletic groups (see Downie and Katz- lack of true vittae in the commissures. On the basis of these Downie 1996, Downie et al. 1996, 2000, 2001, Plunkett et al. findings, several taxa can now be added to or removed from 1996b, Plunkett and Downie 1999). the subfamily, and in most cases these transfers are con- At the subfamilial level, the greatest taxonomic impact of firmed by molecular data. For instance, both matK data recent phylogenetic studies has been the recognition that (Plunkett et al. 1996b) and ITS data (Valiejo-Roman et al. the apiaceous subfamily Hydrocotyloideae is polyphyletic, 2002) indicate that Lagoecia should be removed from with no fewer than three unrelated clades of hydrocotyloids Saniculoideae and placed in Apioideae, and this finding is spread throughout Apiales (e.g. Plunkett et al. 1997, supported by the presence of commissural vittae in Plunkett and Lowry 2001, Chandler and Plunkett 2004) Lagoecia, a feature lacking in all other saniculoids but com- (Figure 1). Of those hydrocotyloids sampled to date, a large mon among the apioids (Liu et al. 2003). Fruit anatomical clade approximates Drude’s original circumscription of this characters also suggest that Saniculoideae should be subfamily, including Azorella, Bolax, Bowlesia,