Naming Clades Using Non-Linnaean Phylogenetic Nomenclature

SAJB-00967; No of Pages 9 South African Journal of Botany xxx (2013) xxx–xxx

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South African Journal of Botany

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Towards a new classiﬁcation of Leguminosae: Naming clades using non-Linnaean phylogenetic nomenclature

Martin F. Wojciechowski ⁎

School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USA article info abstract

Available online xxxx The past three decades of research have greatly advanced our understanding of phylogenetic relationships in the family Leguminosae. It has become clear in recent years that our classification system is in need of signif- Edited by B-E Van Wyk icant updating if it is to reflect our current understanding of the phylogeny of the family and facilitate effec- tive communication of that knowledge. The goal of this paper is to suggest a set of guidelines for formally Keywords: defining and naming clades, which draws on many of the recommendations embodied in the draft Interna- Phylogenetic nomenclature tional Code of Phylogenetic Nomenclature or “PhyloCode”. I provide specific examples of phylogenetic no- Papilionoids Clade definitions menclature applied to several well recognized and well-supported, informally named papilionoid clades to serve as a model for standardizing legume clade names by the legume community in the future. For the most part the clades named here are below subfamily and above tribal ranks in the Linnaean system. It is my contention that a new Linnaean classification, designed to reflect phylogeny, and a clade-based system of phylogenetic nomenclature are mutually complementary approaches to achieving a new classification of the legume family. © 2013 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction legume phylogeny and classification in a more collaborative manner (LPWG, 2013a). As eloquently described by Doyle (in this issue) and LPWG (in this Towards a new classification system for legumes” was the theme issue), the modern era of legume systematics had its origins in the of the Sixth International Legume Conference (ILC6) held at the Uni- landmark series Advances in Legume Systematics, with the publication versity of Johannesburg, in South Africa, January 2013. While signifi- of the first volume edited by Roger M. Polhill and Peter H. Raven cant challenges remain to achieve a comprehensive revision of the in 1981. The intervening 30 years have been especially productive current Linnaean classification (Polhill and Raven, 1981; Polhill, ones for many areas of legume biology, and systematics, in particular, 1994; Lewis et al., 2005; LPWG, 2013a, in this issue), the desire on has made tremendous advances. We are now in a new era of legume the part of the delegates to ILC6 for a new phylogenetically-based systematics, symbolized by the publication of the Legumes of the classification was clearly evident. However, as always the case with World (Lewis et al., 2005), which summarizes the biogeography, phy- contentious or difficult issues, the “devil is in the details”. What was logenetic relationships, and the taxonomy of the family in light of two also clear from discussions at the meeting was that whatever the decades of investigation that have seen a revolution in the kinds and shape of a new Linnaean classification, it will not name and accom- amounts of data coupled with an important conceptual shift in our modate all well-supported clades that merit inclusion, not least be- approaches to inferring evolutionary relationships (e.g., their Fig. 1), cause insufficient ranks exist to accommodate them all, but also and the publication of the first paper authored by the Legume Phylog- because of the requirement under the Linnaean system to name all eny Working Group or “LPWG”, an international coalition of re- taxa at equivalent rank. Nevertheless, clades exist in nature, and searchers working together to tackle the important challenges in knowledge of their relationships and overall place in the phylogeny of the family can be important for accurate communication about legumes. It is my contention, and one that is shared with others, that any new Linnaean classification of legumes, even one that names only monophyletic groups, and an approach that formally defines clades and their overall relationship outside of the traditional Linnae- an framework are not mutually exclusive endeavors, but rather, com- ⁎ Tel.: +1 1 480 727 7767. plementary, and should be utilized together to develop a new legume E-mail address: [email protected]. classification.

Thus, it is important to emphasize that the goal of this discussion 2007: Fig. 1). Although these general categories of clades represent paper is not to establish a clade-based classification system for le- convenient ways of partitioning a nested series of clades, they are gumes that is a competitor to a new, more phylogenetically-based not as useful for defining clades as those based on patterns of survival Linnaean system (e.g., LPWG, in this issue). Rather, my goal here is of lineages to the present time, specifically crown clades and total to outline an approach by which clades can be formally defined so clades (de Queiroz, 2007), as discussed below. as to be incorporated into a new, phylogeny-based Linnaean classifi- Phylogenetic nomenclature has certain advantages over the Lin- cation or a rank-free phylogenetic classification depending on the in- naean system. Under the traditional nomenclatural codes, such as terests of the systematics community. First, I will briefly explain the the ICBN, taxa that are not explicitly associated with a rank cannot concept of phylogenetic nomenclature (e.g., de Queiroz and be formally named. Because phylogenetic nomenclature lacks obliga- Gauthier, 1990, 1992, 1994) and a rationale for using such an ap- tory ranks, taxa can be named without reference to a rank, and there proach to naming clades for use in phylogeny-based classifications. I is essentially no limit to the number of nested clades to which names then review the use of informal names applied to groups in legume can be applied. Furthermore, not only can phylogenetic nomenclature systematics, and how they have been defined (or not). Lastly, I pro- be used in the context of either a rank-based or rank-free classifica- pose guidelines for a formalized approach to naming and defining tion, it does not exclude taxa of known Linnaean rank(s) from inclu- clades in legumes that is based on many of the recommendations of sion in a classification (de Queiroz, 2006). the draft International Code of Phylogenetic Nomenclature (ICPN; Nomenclature can be troubled by ambiguity and inconsistency in Cantino and de Queiroz, 2010). In view of the recognition and repeat- the application of names, such that the same name may have been ap- ed occurrence of a number of strongly-supported legume clades in plied to different groups (monophyletic or non-monophyletic) in dif- many studies, I believe now is an appropriate time to provide formal ferent classifications, which leads to confusion (e.g., de Queiroz and phylogenetic definitions for several of these clades. My hope is that Gauthier, 1994). This can result from the application of priority at a this exercise will serve as a useful model for other legume researchers given rank in traditional rank-based systems or application of the to consider for future naming of clades in their groups of interest, and same name to a different group by different authors. The latter situa- in a manner that aims to bring some standardization to clade names tion has been observed in the use of clade names in the legume liter- that will serve the greater community. ature, for example the definition and membership of the “Robinioid” clade (cf. Lavin et al., 2003 and Wojciechowski et al., 2004). Clearly, 2. Concepts of phylogenetic nomenclature these problems can occur in both rank-based and phylogeny-based nomenclature systems, but one of the most important contributions Biological nomenclature, which is concerned with the naming of offered by phylogenetic nomenclature – linking names explicitly to taxa and the application of taxon names (both existing and newly a particular node, branch or apomorphy – is the potential for greater proposed), is governed by international codes (e.g., the International precision in the application of names, which can promote greater Code of Zoological Nomenclature, Ride et al., 1999; the International clarity in communications about phylogeny (Cantino et al., 2007). Code of Nomenclature for Algae, Fungi and Plants, McNeill et al., Phylogenetic nomenclature is currently not governed by any 2012). These codes, based on the Linnaean system (e.g., Linnaeus, existing code. However, the International Code of Phylogenetic No- 1758), typically require the use of categorical ranks for taxa, many menclature (ICPN) or “PhyloCode” (Cantino and de Queiroz, 2010) of which are mandatory, and the designation of a type specimen, is in development, and is intended to regulate it once it is formally and diagnosis, of an organism to define that taxon, essentially defin- established. Unlike other codes, the ICPN establishes a set of princi- ing taxa and thus their names in the context of taxonomic ranks. ples, recommendations, and rules for nomenclature designed to gov- Under the Linnaean system, taxa that are not explicitly associated ern the names of clades rather than those of ranked groups, which with a rank cannot be formally named, and there is also the require- may or may not correspond to clades (Cantino and de Queiroz, ment to name all taxa at equivalent ranks. This requirement for ranks 2010). The ICPN, while exhibiting a number of important similarities is a major difference between traditional Linnaean and phylogenetic to the traditional rank-based codes, differs fundamentally in using nomenclature and has several complicating consequences for a clade-based definitions for taxon names. phylogeny-based classification. For instance, this requirement limits the number of names that can be assigned in a “nested set” of taxa to no greater than the number of generally recognized ranks, it will 3. Informal clade nomenclature in legumes cause the rank-specific ending of names to change if the rank of the taxon in question changes, and it will inevitably lead to the naming The history of applying informal names to taxa in legumes began of paraphyletic groups. Moreover, recognizing taxa at all the manda- with the Advances in Legume Systematics series and Polhill's (1981b) tory categories may misrepresent their phylogenetic relationships by recognition of informal suprageneric (non-tribal rank), presumably implying the existence of monophyletic groups that do not actually natural, “groups” such as the “Cadia group” or “Sophora group” in exist (de Queiroz and Gauthier, 1992). the papilionoid tribe Sophoreae, on the basis of morphological Phylogenetic nomenclature is a method of naming taxa that re- criteria. Likewise, Barneby and Grimes (1996) often used informal quires an explicit reference to phylogeny, using explicit definitions names to refer to suprageneric groups such as the “Abarema alliance” (de Queiroz and Gauthier, 1990, 1994; see below) that specify taxon and “Pithecellobium alliance” which also do not correspond with tra- names in terms of monophyletic groups and/or common ancestry. ditional tribes. Informal names have also been applied to likely mono- As a result, the application of these definitions leads to explicit hy- phyletic groups identified in early molecular phylogenetic studies, potheses about taxon composition. In other words, phylogenetic no- such as “Neo-Astragalus” (Wojciechowski et al., 1993), the menclature ties names to clades, essentially creating taxa consisting “Astragalean” clade (Sanderson and Liston, 1995), the “Galegoid com- solely of a designated “ancestor” (sensu de Queiroz, 2006; the term plex” (Lavin, 1995), the “50-kb Inversion clade” (Doyle et al., 1997) “ancestral node” is also used) and all of its descendants. Thus, phylo- and many others, which were defined or based primarily on member- genetic nomenclature extends the concept of “tree-thinking” (Baum ship or an apparent apomorphy. In the case of Neo-Astragalus and the and Smith, 2012) to biological nomenclature. 50-kb Inversion clade, membership was first implicated by cytoge- Three general categories of clade definitions, first explicitly recog- netic data (aneuploid chromosome number) or molecular data (re- nized by Hennig (1965), have been employed for phylogenetic no- striction fragment length polymorphisms), respectively, and later menclature: a node-based clade,abranch-based clade, and an corroborated by phylogenetic analyses of DNA sequence data from a apomorphy-based clade (de Queiroz and Gauthier, 1994; de Queiroz, sampling of representative taxa in each group. In neither case was

Please cite this article as: Wojciechowski, M.F., Towards a new classification of Leguminosae: Naming clades using non-Linnaean phylogenetic nomenclature, South African Journal of Botany (2013), http://dx.doi.org/10.1016/j.sajb.2013.06.017 M.F. Wojciechowski / South African Journal of Botany xxx (2013) xxx–xxx 3 the monophyly of these groups supported by any previously recog- similar or identical name in a Linnaean rank-based classification nized morphological or anatomical characters (i.e., “cryptic” clades). (i.e., synonymy). It should also be evident that not all monophyletic In the intervening years, the use of informal clade names has be- groups need to be named, due to a lack of statistical support or for come widely adopted and numerous clades of varying diversity and other reasons, and additional criteria can be used to decide what distinction have been described among caesalpinioid (e.g., “Prioria” clades to name. Criteria such as whether the taxon is easily diagnos- and “Afzelia” clades: Bruneau et al., 2008), mimosoid (e.g., able, whether it is well-established in the literature or named tradi- “Botrycephalae” and “Pulchelloidea” clades: Murphy et al., 2010), tionally, and whether nomenclatural changes are minimized by and papilionoid legumes (e.g., “Adesmia”, “Dalbergia”, and naming a taxon should be considered in the decision to name a “Pterocarpus” clades: Lavin et al., 2001). Our knowledge of the phylo- clade (Backlund and Bremer, 1998; Stevens, 2012). genetic relationships of many legume groups has now advanced to A format for the formal naming of clades recognized in legume the point where, for example, the majority of subfamily phylogeny is suggested below. Clades are defined and named essen- Papilionoideae can be resolved into a number of larger and smaller tially in accordance with the fundamental rules of phylogenetic no- clades and individual lineages (Cardoso et al., 2012, this issue). Unfor- menclature that govern choice of names, definition types and tunately, there are instances where different names have been ap- specifiers, attribution of authorship outlined in the ICPN (Cantino plied to the same clade or the same name has been applied to and de Queiroz, 2010), some of which are explained below. It is im- different clades, with often varying degrees of definition from virtual- portant to note that the ICPN has not yet been published (currently ly none to minimally informative statements such as “the X clade is in draft form), and in some cases, critiques that might be considered delimited by the most recent common ancestor of taxon Y and in its future development are noted. For a more complete description taxon Z” (e.g., Wojciechowski et al., 2004). To avoid these issues, rec- of the ICPN and an explanation of its rules, consult Cantino and de ognized protocols for the standardization of clade definitions and Queiroz (2010);(http://www.ohio.edu/phylocode/). names are needed. It is worth noting that no legume studies to date have attempted to incorporate or assimilate these, or any other, informally named clades within the traditional rank-based system that is 4.1. Clade definition required by the existing botanical code, or as formally defined clades according to the requirements of any code, beyond the minimal To be more formally established under ICPN rules, a name must be ‘crown clade definitions’ of Wojciechowski et al. (2004: 1851). provided with a phylogenetic definition, linking it explicitly to a par- A variety of named clades are found in numerous other plant ticular crown or total clade. A crown clade is a clade originating from groups. In many groups (e.g., angiosperms, APG, 1998, 2003, 2009; the most recent common ancestor of two or more extant taxa (spe- Compositae, Funk et al., 2009; Campanulidae, Tank and Donoghue, cies or other taxon), whereas, a total clade is a clade comprised of a 2010) the composition of existing Linnaean ranks has been modified crown clade and all species and/or other taxa that share a more recent or redefined to more accurately represent strongly-supported clades common ancestor with that crown clade than with any other mutual- identified in phylogenetic analyses. Other good examples of this ap- ly exclusive crown clade (de Queiroz, 2007: Fig. 2), as illustrated in proach include the phylogenetic reclassification of fungi (Hibbett et Fig. 1. Three kinds of definitions can be used to specify a crown al., 2007) and the recently updated phylogeny of angiosperms clade: (1) a node-based definition, (2) a branch-modified (Soltis et al., 2011) which incorporates many clades formally named node-based definition, and (3) an apomorphy-modified node-based using nomenclature conventions based on the PhyloCode (Cantino definition, although this list of options is not exhaustive (Cantino et et al., 2007). However, the option of defining and naming one or al., 2007; de Queiroz, 2007). These definitions represent slightly dif- more robustly supported clades that may not be covered by any ferent ways of specifying the ancestor (see ICPN, Art. 2) or ancestral rank-based names, using either Latinized or non-Latinized names, node, and once this ancestor or ancestral node is specified, the defini- has been favored by systematists for other plant groups. As an exam- tion and thus the meaning of the name are fixed. In such definitions, ple, the Grass Phylogeny Working Group (2011) produced a robust the ancestor is described by its relationship to two or more “speci- phylogeny of Poaceae that has been used to a refine a fiers”, taxa which may be internal or external, relative to the clade it- phylogeny-based classification incorporating both formal Linnaean self. Taxa identified as specifiers may be designated explicitly (e.g., and informal clade names, one which effectively serves as the “taxon- Vicia faba L.) or described as any member of another more exclusive omy” of the family in the NCBI Taxonomy Browser (http://www.ncbi. taxon (e.g., genus Andira Lam.) in the definition, and may either be nlm.nih.gov/Taxonomy/Browser/wwwtax.cgi?id=4479). Though in- extant or extinct depending on the particular phylogeny (i.e., based formal clade names are widespread in angiosperm phylogenies (e.g., on molecular or morphological data, or both) on which the definition “eudicots” and “rosids”, AGP, 1998, 2003, 2009; “PACMAD” in the is based. Comments on the name and/or its definition should be grass phylogeny, GPWG, 2011), in most cases informal names such added to clarify the origin and history of the name if it already exists as these have not been incorporated into new, formal Linnaean clas- (i.e., a “preexisting” name, see below). sifications of those groups. In this paper I give formal names to clades subject to the same rules of priority, etc. as formal names in a rank-based system. 4. Proposal for formal naming of legume clades According to the ICPN, new formal names for such clades are single words that are capitalized and Latinized (Cantino and de Queiroz, A well-supported hypothesis of monophyly is a necessary prereq- 2010). However, such Latinized clade names may cause confusion uisite for a group to be formally defined and named (although it may with Linnaean names, and for some users these names may carry con- not be sufficient). As a related convention, any group can be recog- notations of Linnaean ranks, even though there are none implied. Al- nized with an informal name but only monophyletic groups are to though it is currently a convention of the draft ICPN that all be recognized with formal names. Monophyletic groups may be re- “established names with priority” must be Latinized (ICPN, Art. 17), ferred to using the word ‘clade’ as part of the informal name, e.g., one could argue that any clade name could be applied and stand (be “Cercideae clade” or “IR-lacking clade” to distinguish them from conserved) given the rule of priority. This is one of those contentious non-monophyletic or paraphyletic taxa. Paraphyletic taxa should issues which deserve future debate in the phylogenetic continue to be referred to as a ‘grade’, as in the “caesalpinioid nomenclature-classification community. Given the likely confusion grade”, to distinguish them from monophyletic taxa. The use of the that use of Latinized clade names will generate between ICPN-based word “clade” as part of the name can further serve to distinguish names and Linnaean names, plus the fact that many legume clades al- that taxon from any taxon currently, or in the past, named with a ready have informal non-Latinized names that are widely used and

Crown clade = To most closely Papilionoideae related caesalpinioid crown clade crown node

Time Time side branch

Total clade = stem lineage Pan-Papilionoideae

Fig. 1. Crown clades and total clades (modified from de Queiroz, 2007), to illustrate the relationship of Papilionoideae and Pan-Papilionoideae clades, respectively. Lineages having extant descendants are represented as black branches, while those lacking extant descendants are shown as gray branches. understood, I have chosen here to retain those names in the clade, and any feature that is derived within the clade but is not non-Latinized form for several clades. diagnostic of the clade per se. A clade name governed by the ICPN may be “new” or “converted”, “ ” depending upon whether the name is preexisting or not. 4.4. Composition, biogeography, importance Preexisting names are typically scientific names that are either (a) le- gitimately established under the ICBN or other traditional codes, or A short description of the diversity and importance of the clade (b) names that are in current use but not governed by any code at in terms of number of genera/species, biogeographic distribution the time they were published, and have never been published with (present and past, if known), unique or noteworthy paleobotanical a Latin diagnosis (although this is no longer a requirement under evidence, and ecological and economic uses of the members of the the ICBN), provided they have been published with a description or clade may be included. diagnosis in some other language (e.g., defined phylogenetically in publications; see ICPN Art. 6.2 and Note 6.2.1) prior to their establishment under the ICPN. A new clade name is a name that has not previ- 4.5. Synonymy and etymology ously been used for the clade, or any other taxon (e.g., Pan-Papilionoideae, see below), while a converted clade name is a Synonym(s), whether established previously under a rank-based preexisting name (e.g., Hologalegina, see below) that has been code, or those that are in current or recent use but not provided established by publishing a formal phylogenetic definition for it with a Latin diagnosis, or informal names applied to the same taxon, (Cantino and de Queiroz, 2010). For the converted clade names treat- should be indicated. In addition, the etymology of the name that cor- fi ed below, the definitional author(s) is cited in square brackets to dis- responds to the taxon as de ned may be described. tinguish that author(s) from the nominal author(s) (creator of the name) of the clade as appropriate. 5. Toward a phylogenetic nomenclature for Papilionoideae

There would be considerable advantages in developing a 4.2. Reference phylogeny clade-based naming system that is consistent and supported by a broad consensus of the legume systematics community, such that In order for a clade name to be formally established, the definition new names would carry the authority of the recently formed LPWG, must include complete citation of an appropriate reference phylogeny and hence, would have a greater chance of gaining widespread accep- (or phylogenies), which specifies the clade's definition, composition tance and use. Using the consensus papilionoid phylogeny of Cardoso and its relationship to sister or closely related taxa. While all relevant et al. (2012, this issue), I provide formal phylogenetic definitions and studies for each group need not be cited, the analysis chosen as min- names for selected clades as examples of such a naming system. This imum documentation for the monophyly of the group should be that is intended as a model that the legume community might wish to which has the largest number of taxa and/or characters (e.g., molecu- consider for formally defining and naming clades, either in the con- lar loci or morphological features), provides the strongest statistical text of a new Linnaean classification, or as the basis of a support (expressed as bootstrap proportions and/or Bayesian posteri- non-Linnaean phylogenetic classification for the entire legume or probabilities), and apomorphy(ies) where appropriate, that sup- family. port the monophyly of the taxon in question. Taxa that are named Several of the clades that I have chosen to formally define and should be well-supported as monophyletic by at least one published name as examples here were identified and informally named in pre- phylogenetic analysis, although this is not applicable for monotypic viously published studies by this author (with indicated co-authors). taxa. All clades have strong statistical support based on molecular phylogenetic analysis (e.g., N90% bootstrap proportions and N0.95 Bayesian posterior probabilities), often from more than one data set, and sever- 4.3. Diagnostic apomorphy(ies) al of them are marked by molecular and/or morphological apomorphies. The example clades named below include some that Diagnostic anatomical and morphological apomorphy(ies) for comprise several current Linnaean tribes (e.g., “Hologalegina”), and the clade may be described as appropriate, especially in the case these are the most likely candidates to be integrated into a of apomorphy-based definitions, including any unique molecular, non-Linnaean classification. Other examples, such as “Papilionoideae”, biochemical, cytogenetic or developmental evidence supporting the are likely to be recognized as a subfamily in a Linnaean classification, monophyly of the taxon. This list may include a description of any and would therefore be much less likely to be included in a mixed features, which, in combination, present a diagnostic syndrome for Linnaean and formally defined clade scheme.

Pan-Papilionoideae M. F. Wojciechowski, new clade name. Reference phylogeny: Wojciechowski et al. (2004; Fig. 2) and Definition: The total clade or “panclade” (i.e., crown plus stem, Wojciechowski (2013; Fig. 2). See also Doyle et al. (1997; Fig. 1), sensu de Queiroz, 2007) of Papilionoideae (defined below). There is Pennington et al. (2001; Fig. 1), Cardoso et al. (2012; Fig. 3), which no preexisting scientific established under the ICBN, or informal present evidence for less inclusive versions of this clade. name, for this clade. Composition: The genera Cladrastis Raf. 1824 (six spp.), Pickeringia Reference phylogeny: Cardoso et al. (2012; Figs. 2, 3). Nuttall 1840 (monotypic), and Styphnolobium Schott 1830 (nine spp.) Composition: Papilionoideae, and all extinct taxa that share more comprise this clade. Both Cladrastis and Styphnolobium show an inter- recent ancestry with Papilionoideae than with extant caesalpinioid esting pattern of northern hemisphere disjunction, distributed in and mimosoid legumes. eastern Asia and southern North America, while Pickeringia is restrict- Synonymy: None. ed to California and northern Baja California. Several taxa described as species of Cladrastis and Styphnolobium are known from the fossil re- Papilionoideae (L.) DC. [M. F. Wojciechowski], converted clade cord (Herendeen, 1992). name. Synonyms: Cladrastis clade (informal). Definition (branch-modified, node-based): The most inclusive crown clade containing Castanospermum australe A. Cunn. ex Mudie Meso-Papilionoideae L. P. de Queiroz and M. F. Wojciechowski, 1829 and Vicia faba L. 1753 but not Caesalpinia gilliesii (Wall. ex new clade name. Hook.) D. Dietr. 1840, Gleditsia triacanthos L., or Dialium guianense Definition (apomorphy-modified, node-based): The most inclu- (Aubl.) Sandwith 1939. Because sister group relationships are better sive crown clade exhibiting the structural rearrangement in the plas- resolved and supported than basally-branching ingroup relationships tid genome (inversion of a ~50 kb segment in the large-single copy within this clade, a branch-modified node-based definition was used region with endpoints between the accD and trnK regions; Doyle et to maximize definitional and compositional stability (Cantino et al., al., 1996) homologous with that found in Aldina latifolia Spruce ex 2007). Benth. 1870, Holocalyx balansae Micheli 1883, Maackia amurensis Comments on name. Papilionoideae (L.) DC. 1825 is a preexisting Rupr. 1856, Wisteria floribunda (Willd.) DC. 1825, and Glycine max scientific name established under the rank-based ICBN and applied (L.) Merr. 1917, where these taxa are extant species included in the to the subfamily of the Leguminosae Jussieu 1789 that corresponds crown clade defined by this name. There is no preexisting scientific to this clade. Faboideae Rudd 1968 is an alternative name for this sub- name for this taxon. The name “50-kb Inversion clade” (Doyle et al., family of Fabaceae Lindl. 1836 or Leguminosae, whereas the similar 1997) was not explicitly defined phylogenetically. The prefix Papilionaceae Giseke 1792 is the appropriate name for this taxon “meso-”, meaning “middle”, is used here to refer to this taxon as a when the subfamily is treated as a separate family from less inclusive clade (i.e., more derived or nested within) in relation the Caesalpiniaceae R. Br. 1814 and Mimosaceae R. Br. 1814. to the more inclusive reference clade Papilionoideae (see Cantino et Reference phylogeny: Cardoso et al. (2012; Fig. 1). The monophyly al., 2007, for usage). of Papilionoideae has been demonstrated in all higher-level molecular Reference phylogeny: Cardoso et al. (2012; Figs. 4–7), see phylogenetic analyses published to date beginning with Käss and also Doyle et al. (1996) for listing of taxa shown to possess this Wink (1996) and Doyle et al. (1997), albeit sometimes without ro- rearrangement. bust statistical support. Later analyses such as Wojciechowski et al. Diagnostic apomorphy: This structural rearrangement – the 50-kb (2004; Fig. 2) and Cardoso et al. (2012; Fig. 3) have provided un- inversion – was initially identified by restriction fragment length equivocal, robust support for this clade. polymorphism analyses of plastid DNA from a large number of le- Diagnostic apomorphy: Flowers generally zygomorphic, or some gumes species (Doyle et al., 1996). Subsequently, the monophyly of actinomorphic, adaxial petal generally outside the adjacent lateral this group has been corroborated by almost all cladistic analyses of petals, sepals generally united at base. variation in molecular sequence data (e.g., Doyle et al., 1997; Composition: This clade, comprised of more than 478 genera and Pennington et al., 2001; Wojciechowski et al., 2004; Cardoso et al., 13,800 species (Lewis et al., 2005), is cosmopolitan in distribution 2012), although strong statistical support has been lacking. and includes the vast majority of agriculturally important legumes Composition: This clade, marked by the inversion of a 50-kb region in such as Pisum sativum L. (pea), Medicago sativa L. (alfalfa), Trifolium the plastid genome, contains the majority of papilionoid legumes includ- L. (clovers), Vicia L. (vetches), Lens Mill. (lentils), Lupinus L. (lupins), ing the three main large radiations of papilionoids, the Genistoids s.l., Glycine max (L.) Merr. (soybean), Phaseolus L. (beans), Lablab Dalbergioids s.l., and a clade comprising the majority of Papilionoideae purpureus (L.) Sweet (hyacinth bean), and Arachis hypogaea L. that includes the Baphioid and Non-Protein-Amino-Acid-Accumulating (peanut). clades (Cardoso et al., 2012, this issue). Synonyms/Etymology: Papilionoideae (L.) DC. 1825, Faboideae Synonyms: 50-kb Inversion clade (informal). Rudd 1968, and the informal name “Papilionoids”. The name “papilionoid” most likely comes from the resemblance of the typical Vataireoid clade R. T. Pennington, M. Lavin, H. Ireland, B. B. or characteristic flower to a butterfly(papilio, from Latin), especially Klitgaard, J. Preston, and J.-M. Hu [M. F. Wojciechowski], converted when the flower is dissected into its component five petals. clade name. Definition (branch-modified, node-based): The most inclusive Cladrastis clade M. F. Wojciechowski, M. Lavin and M. J. Sanderson crown clade containing Sweetia fruticosa Spreng. 1825 and Vatairea [M. F. Wojciechowski], converted clade name. guianensis Aubl. but not Andira inermis (W. Wright) DC., Zollernia Definition (branch-modified node-based): The most inclusive ilicifolia (Brongn.) Vogel 1837, or Aldina insignis (Benth.) Endl. 1843. crown clade containing Cladrastis kentukea (Dum. Cours.) Rudd There is no preexisting scientific name for this clade. The name 1971 but not Dermatophyllum secundiflorum (Ortega) Gandhi & Re- “Vataireoid clade” was not explicitly defined phylogenetically veal 2011 or Swartzia simplex Spreng. 1825. There is no preexisting (Pennington et al., 2001), nor does the name meet the other require- scientific name for this taxon. The name “Cladrastis clade” was not ex- ments for establishment (under either the ICBN or ICPN). In spite of plicitly defined phylogenetically (Wojciechowski et al., 2004), nor this, the name qualifies as a ‘preexisting’ name under the ICPN (Art. does the name meet the other requirements for establishment 6.2 b) as “a name that is in use but not governed by any code”. How- (under either the ICBN or ICPN). In spite of this, the name qualifies ever, Pennington et al. (2001) erroneously applied this name to a as a ‘preexisting’ name under ICPN article 6.2 b as “a name that is in larger, more inclusive clade (i.e., including the genera Exostyles Schott use but not governed by any code”. 1827 and Harleyodendron R. S. Cowan 1979), while Wojciechowski

Please cite this article as: Wojciechowski, M.F., Towards a new classification of Leguminosae: Naming clades using non-Linnaean phylogenetic nomenclature, South African Journal of Botany (2013), http://dx.doi.org/10.1016/j.sajb.2013.06.017 6 M.F. Wojciechowski / South African Journal of Botany xxx (2013) xxx–xxx et al. (2004) and Mansano et al. (2004) found support for a less inclu- homologous with that found in Galega officinalis L. 1753, Glycyrrhiza sive clade. lepidota Nuttall 1813, and Vicia faba L., where these taxa are extant Reference phylogeny: Cardoso et al. (2012; Fig. 4) and Cardoso species included in the crown clade defined by this name. There is et al. (2013; Fig. 1). no preexisting scientific name for this clade. The name “IR-Lacking Composition: The genera Luetzelburgia Harms 1922 (8 spp.), Sweetia Clade” or “IRLC” (Wojciechowski et al., 2000) was not explicitly de- Spreng. 1825 (1 sp.), Vatairea Aubl. 1775 (8 spp.), and Vataireopsis fined phylogenetically nor does the name meet the other require- Ducke 1932 (4 spp.), distributed primarily in northern South America ments for establishment (under either the ICBN or ICPN). In spite of (French Guiana to Brazil to Bolivia; Lewis et al., 2005), comprise this this, the name qualifies as a ‘preexisting’ name under the ICPN (Art. clade. Species of Vatairea and Vataireopsis are important sources of 6.2 b) as “a name that is in use but not governed by any code”. The woods and medicinals (Klitgaard and Lavin, 2005). “IR-Lacking Clade” or “IRLC” corresponds to the “temperate herbaceous clade” of Sanderson and Wojciechowski (1996), and is equiva- Dalbergioid s.l. clade M. F. Wojciechowski, M. Lavin and M. J. lent to what might be termed “Galegeae sensu lato” (sensu Polhill, Sanderson [M. F. Wojciechowski], converted clade name. 1981a), a paraphyletic group we now know contains various other Definition (node-based): The least inclusive crown clade that con- predominantly temperate, herbaceous tribes (Carmichaelieae, tains Amorpha fruticosa L. 1753 and Dalbergia sissoo Roxb. ex DC. Cicereae, Fabeae, Hedysareae, Trifolieae) nested within it. 1825. There is no preexisting scientific name for this clade. The Reference phylogeny: Wojciechowski et al. (2000; Figs. 1, 2) and name “Dalbergioid s.l. clade” was not explicitly defined phylogeneti- Wojciechowski et al. (2004; Fig. 5). See also Käss and Wink (1996; cally (Wojciechowski et al., 2004), nor does the name meet the Fig. 1), Sanderson and Wojciechowski (1996; Fig. 3), Doyle et al. other requirements for establishment (under either the ICBN or (1997; Fig. 1), and Pennington et al. (2001; Fig. 1) for additional ICPN). In spite of this, the name qualifies as a ‘preexisting’ name supporting evidence. under the ICPN (Art. 6.2 b) as “a name that is in use but not governed Diagnostic apomorphy: This clade was the first monophyletic group by any code”. See also Cardoso et al. (2012). of legumes to be distinguished by a molecular synapomorphy, the loss Reference phylogeny: Wojciechowski et al. (2004; Fig. 3). See also of one of two copies of the 25-kb inverted repeat in the plastid genome. McMahon and Hufford (2004; Figs. 1, 3) for Amorpheae and Lavin This structural mutation was initially identified by restriction fragment et al. (2001; Fig. 5) for “Dalbergioid clade”. See also Cardoso et al. length polymorphism analysis of plastid DNA from a large number of le- (2012; Fig. 7). gumes species (Lavin et al., 1990). Subsequently, the monophyly of this Composition: The Dalbergioid clade (Lavin et al., 2001), with 45 group has been corroborated by additional DNA fragment analysis genera and ~1270 species of trees, shrubs, perennial and annual (Liston, 1995), and supported by all cladistic analyses of variation in herbs is distributed pantropically, especially in the Neotropics and molecular sequence data (e.g., Sanderson and Wojciechowski, 1996; sub-Saharan Africa (Klitgaard and Lavin, 2005), and tribe Amorpheae Doyle et al., 1997; Wojciechowski et al., 2004). Boriss. 1964, with eight genera and ~240 species, distributed from Composition: This clade, with over 4380 species, corresponds ap- the southwestern USA and Mexico to northern Argentina, comprise proximately to Polhill's (1981a) “temperate herbaceous group”, com- this clade. prising all members of tribes Cicereae Alef. 1859, Galegeae Dumort. Synonyms: Dalbergioid s.l. clade (informal). 1827 (incl. Carmichaelieae; Lock and Schrire, 2005), Hedysareae DC. 1825, Trifolieae Endl. 1830, and Vicieae DC. 1825 (= Fabeae Hologalegina M. F. Wojciechowski, M. J. Sanderson, K. P. Steele, and Rchb. 1832), as well as a “millettioid group” of genera (Schrire, A. Liston [M. F. Wojciechowski], converted clade name. 2005) that includes Afgekia Craib 1927, Callerya Endl. 1843, Definition (node-based): The least inclusive clade containing As- Endosamara R. Geesink 1984, Sarcodum Lour. 1790, Wisteria tragalus canadensis L. 1753, Robinia pseudoacacia L. 1753, Sesbania Nutt.1818, and possibly Antheroporum Gagnep. 1915. grandiflora (L.) Pers. 1807, and Vicia faba L. 1753. The name Synonyms: IR-Lacking clade or IRLC (informal). “Hologalegina” was first applied to the monophyletic group defined as consisting exclusively of the “IR-lacking clade”, the genus 6. Phylogenetic classification of the Papilionoideae: Sesbania Scop., and tribes Loteae DC., and Robinieae Hutch. a rank-free example (Wojciechowski et al., 2001, 2004). The name “Hologalegina” was not explicitly defined phylogenetically, nor does the name meet Below I present an example of a phylogenetic classification the other requirements for establishment (under either the ICBN (rank-free) of papilionoid legumes (Fig. 2) based on the higher-level or ICPN). In spite of this, the name qualifies as a ‘preexisting’ name phylogeny presented in recent papers by Cardoso et al. (2012, this under the ICPN (Art. 6.2 b) as “a name that is in use but not governed issue), which includes both formal and informally named clades and by any code”. names of recognized Linnaean suprageneric taxa (e.g., tribe) and gen- Reference phylogeny: Wojciechowski et al. (2004; Fig. 5). See also era. In this example, all taxa listed have been included without regard Wojciechowski et al. (2000; Figs. 1, 2). to their level of support as determined by phylogenetic analyses. Au- Composition: This clade, with over 4800 species, consists of the thor(s) references for each of the clade names (formal and informal) vast majority of legumes presently distributed in temperate regions are given in parentheses while formal Linnaean rank-based names in- of the world, includes the tribes Loteae (sensu Polhill, 1994) and clude standard authorities. Names with “Cardoso et al., this issue” indi- Robinieae (sensu Lavin and Schrire, 2005), and the “IRLC” cated as the author, are proposed tribal names (Cardoso et al., in this (Wojciechowski et al., 2000). issue). Lineages represented by a single sampled species (e.g., Etymology: The name was chosen to reflect the fact that this clade Amphimas pterocarpoides Harms) include the complete species name contains all taxa that have been variously treated (at generic and whereas a lineage represented by two or more (potentially) species of subtribal levels) under the tribe Galegeae Dumort. 1827. a genus (e.g., Aldina Endl.) is indicated by generic name only. Taxa of un- Synonyms: Hologalegina (informal). certain position relative to defined clades or formally ranked taxa are listed as incertae sedis, and have been placed in the least inclusive IR-lacking clade M. F. Wojciechowski, M. J. Sanderson, K. P. Steele, clade in the hierarchy where they can be assigned with confidence. and A. Liston [M. F. Wojciechowski], converted clade name. Monophyletic groups that have not been named in any known publica- Definition (apomorphy-modified, node-based): The most inclu- tion (to my knowledge) are so indicated. Synonymy (both formal and sive crown clade exhibiting the structural mutation in the plastid ge- informal) is indicated where appropriate. *Asterisk indicates clades for- nome (loss of one copy of the ~25-kb inverted repeat region) mally defined and named in this paper.

Pan-Papilionoideae* (M. F. Wojciechowski) Papilionoideae* (M. F. Wojciechowski) = subfamily Papilionoideae(L.) DC. 1825 ADA clade (Cardoso et al., 2012) Angylocalyceae(Cardoso et al., 2013b) = Angylocalyxclade (Cardoso et al., 2012) Dipterygeae(Cardoso et al., 2013b) = Dipterygeaeclade (Cardoso et al., 2012) Amburaneae(Cardoso et al., 2013b) Unnamed monophyletic group Swartzieae(Cardoso et al., 2013b) = Swartzioidclade (Torkeand Schaal, 2008) Ateleoidclade (Ireland et al. 2000) Swartzioids.s.clade (Ireland et al., 2000) Unnamed monophyletic group Cladrastisclade * (M. F. Wojciechowski) = Cladrastisclade (Wojciechowskiet al., 2004) Meso-Papilionoideae* (L. P. de Queirozand M. F. Wojciechowski) = 50-kb Inversion clade (Doyle et al., 1997) Amphimaspterocarpoides Harms [incertaesedis ] Aldina Endl. [incertaesedis ] Dermatophyllum Scheele [incertaesedis ] Exostyleae(Cardoso et al., 2013b) = Lecointeoidclade (Cardoso et al., 2012) Vataireoidclade * (M. F. Wojciechowski) = Vataireoidclade(Pennington et al., 2001) Andiraclade (Cardoso et al., 2012) Genistoids.l. clade (Wojciechowskiet al., 2004) Ormosieae(Cardoso et al., 2013b) = Ormosiaclade (Cardoso et al., 2012) Clathrotropismacrocarpa Ducke[ gen. nov.] Brongniartieae(Ross and Crisp, 2005) Leptolobieae(Cardoso et al., 2013b) = Bowdichiaclade (Cardoso et al., 2012) Core Genistoidclade (Crisp et al., 2000) Camoensieae(Cardoso et al., 2013b) Unnamed monophyletic group Sophoreae(Cardoso et al., 2013b) Unnamed monophyletic group Podalyrieae(Cardoso et al., 2013b) Unnamed monophyletic group Crotalarieae(Benth.) Hutch. Genisteae(Bronn) Dumort. Dalbergioids.l. clade * (M. F. Wojciechowski) = Dalbergioids.l. clade (Wojciechowskiet al., 2004) AmorpheaeBoriss. Amorphoidclade (McMahon and Hufford, 2004) Daleoidclade (McMahon and Hufford, 2004) Dalbergieae(Cardoso et al., 2013b) = Dalbergioidclade (Lavin et al., 2001) Unnamed monophyletic group Baphieae(Cardoso et al., 2013b) = Baphioidclade (Pennington et al., 2001) Non-Protein Amino Acid-Accumulating clade (Cardoso et al., 2012) = Canavanine-accumulating clade (Wojciechowskiet al., 2004) Mirbelioidclade (Wojciechowskiet al., 2004) Unnamed monophyletic group Indigofereae(Schrireet al., 2009) = Indigoferoidclade (Cardoso et al., 2012) Millettioidclade (Hu et al., 2000) Hologalegina* (M. F. Wojciechowski) = Hologalegina(Wojciechowskiet al., 2000) Robinioidclade (Wojciechowskiet al., 2004) IR-lacking clade* (M. F. Wojciechowski) = IR-Lacking clade (Wojciechowskiet al., 2000)

Fig. 2.

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