The recent history of Compositae systematics: from daisies to deep achenes, sister groups and metatrees

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1 Chapter 2 The recent history of Compositae systematics: from daisies to deep achenes, sister groups and metatrees Vernon H. Heywood INTRODUCTION The early history of Composite taxonomy and systematics has been covered in the introductory chapter up to the Proceedings of the 1975 symposium at the University of Reading, UK, entitled An overture to the Compositae (Heywood et al. 1977) and in the present contribution (Chapter 1), so I shall focus on advances in the subsequent twenty-five to thirty years during which we have witnessed a radical transformation of approaches to taxonomy and systematics and our understanding of phylogenetic relationships. Added to that have been drastic changes in the environmental, social and economic circumstances in which we practice our science. THE SITUATION IN 1975 Life was exciting for taxonomists in the 1970s when the first Compositae symposium was held at Reading. The classification of the flowering plants was in a period of transition. Technical advances such as electron microscopy and analytical chemical techniques led to the production of new data from micromorphology, palynology and the chemistry of secondary compounds, and at the species and population level, the future direction of biosystematics and genecology was being debated Biosystematics at the crossroads was the title of a symposium at the Seattle Botanical Congress in 1969, reflecting doubts about the validity of the biological species concept on both theoretical and practical grounds. At that time, phenetic taxonomy/classification, with its emphasis on quantification of characters and character states, was part of an attempt to make the procedures of classification more explicit and reproducible, and numerical phenetics (numerical or Adansonian taxonomy) was being increasingly used to handle large datasets being produced, within the limitations of the then existing computing technology and instrumentation. Sokal and Sneath s Principles of Numerical Taxonomy (1963) was a highly influential text in this field and was updated as Sneath and Sokal s Numerical Taxonomy : The Principles and Practice of Numerical Classifi cation (1973). Davis and Heywood s Principles of Angiosperm Taxonomy, which was also published in 1963, was not only the first textbook to provide a detailed analysis of the principles, issues and concepts of plant taxonomy but was essentially phenetic in its philosophy. The phenetic approach was distinguished from the rather vague concept of evolutionary systematics sensu Mayr and from the emerging cladistic approach that was beginning to be espoused. Subsequently, during the 1960s and 1970s there was an almost endless debate regarding the relevant merits of phenetic and phylogenetic taxonomy in journals such as Systematic Zoology. Today

2 40 Heywood the relevance of phenetic classification has been largely dismissed and often, wrongly, considered as anti-evolutionary (see discussion in Stevens, 2000) although some (myself included) would argue that it still has a significant role to play in taxonomy. The widely used systems of classification of the flowering plants such as those of Cronquist (1968, 1981), Takh tajan (1969, 1997), and Thorne (1976, 2000, s.d.), avowedly incorporated evolutionary principles, but without using any explicit methodology and with little documentation of the processes involved or the information base used in reaching the conclusions adopted. Yet these and earlier systems, whether phylogenetic or not, such as those of Bessey, Bentham and Hooker, Engler, because of their recognition, description and delimitation of families (and in some cases subfamilies and tribes) provided (and still provide) the context which made later cladistic systems possible and comprehensible. The phylogenetic approach of Hennig, although vigorously advocated by some, was at that time still little known and only slowly made any impact in botany. Likewise, biochemical systematics was then based largely on secondary compounds, and was just venturing into the macromolecular phase. In the Biology and Chemistry of the Compositae (Heywood et al. 1977), mention is made of the early results of Boulter and his colleagues on amino acid sequences in the family, another neglected area, as it was called, and in his summary of the chemistry of the family, B.L. Turner was of the opinion that at the level of the tribe and above as such macromolecules would provide the only meaningful (or convincing) data! None of the new approaches made much impact on the classification of the flowering plant families, although the circumscription and relationships of some families was affected to some extent, and no new system of classification was produced. When I produced Flowering Plants of the World (Heywood 1978), the sequence of families used followed that of Stebbins in his Flowering Plants Evolution Above the Species Level (1974), itself largely based on Cronquist s 1968 system, but with the prophetic remark in the Preface, it is likely that future systems will be radically different. The treatment of the Compositae in that volume was by Charles Jeffrey (1978) who noted that the classification of the family was in a state of transition and that the arrangement into two subfamilies and twelve tribes was seen to be in need of modification in the light of new evidence. RECENT MILESTONES IN COMPOSITAE CLASSIFICATION AND PHYLOGENY Curiously, one of the most widely cited papers on Com - positae systematics even today is Cronquist s The Compositae revisited (1977) which was in fact given at the 1977 symposium but which could not be included in the published volume. Major developments since then include: The retreat from the traditional division of the family into two large subfamilies, the Cichorioideae and the Asteroideae, in favor of the recognition, based on both morphological and phylogenetic analyses of two very unequal sister groups: a small Barnadesioideae which is sister to the rest of the family which constitute the Asteroideae and a more narrowly circumscribed Cichorioideae. The publication of Bremer s Asteraceae: Cladistics & Classifi cation (1994) which was described as a bible or perhaps new testament for the then current generation of Compositae students. It provided a first approximation of a phylogenetic system of classification of the family and an invaluable data source. The International Compositae Conference, held at Kew, 1994 just after publication of Bremer s book, and the Proceedings from it which covered both reviews and syntheses of the systematics and evolution of the family and its major component taxa (vol. 1. Com positae: Systematics, eds. D.J.N. Hind and H.J. Beentje, 1995) and a wide range of more applied aspects (vol. 2. Compositae: Biology and Utilization, eds. P.D.S. Caligari and D.J.N. Hind). The significance of molecular studies in the classification of the family was only just beginning to be realized at the time of this meeting (cf. Jansen and Kim 1996) and as Funk et al. (2005) note, the work of Jansen and colleagues ( Jansen and Palmer 1987, 1988) on chloroplast DNA in the late 1980s led to the biggest change in Compositae systematics till then, and, as they say, literally turned the Compositae phylogeny upside down, showing that part of the Mutisieae was the basal branch of the family and that the tribe Heliantheae s.l. was nested far up in the tree. Furthermore, their work showed that Vernonieae and Eupatorieae, long believed to be closely related, were actually in separate parts of the tree. The publication of new morphological and molecular studies led to further substantial reassessment of evolutionary relationships within Compositae and a new phylogenetic classification of the family was published by Panero and Funk (2002), recognizing ten subfamilies and thirty-five tribes. Then, by synthesizing a tree of the family and published and unpublished trees within the family, Funk et al. (2005) were able to produce a supertree or metatree that reflects much of the currently held views about the relationships among the major tribes and subfamilies in Compositae. The publication of the treatment of Compositae in Kubitzki s The Families and Genera of Vascular Plants

3 Chapter 2: The recent history of Compositae systematics 41 (Anderberg et al. 2007) in which over 1620 genera in thirty tribes are recognized. Compositdb a database of molecular data for the Compositae species. A collaboration between the lab oratories of Steve Knapp at Oregon State Univer sity and Richard Michelmore at UC Davis. It was initially funded by USDA ARS but is currently without support. Primarily focused on sunflower and lettuce but will expand it to include any Compositae species for which there is sufficient data and interest. It is to be hoped that this initiative will receive greater support and become more closely associated with the International Compositae Alliance. The proposed Global Working Checklist of Compositae. For details see the TICA Website. This recent development is a response to the need for family catalogues as part of the attempt to meet Target 1 of the Global Initiative for Plant Conservation which aims to produce a widely accessible working list of known plant species, as a step towards a complete world flora. and the Global Working Checklist of Compositae BIF seed Funding Project Newsletter 2, November Christina Flann has now received three years of funding for this project and has taken the lead on bringing it to completion. REVOLUTIONS IN TAXONOMY AND SYSTEMATICS Over the past twenty years a major shift, some would say a quantum shift, has taken place in plant taxonomy and more especially systematics. This has been as the result of: the publication of a large number of papers detailing morphological, anatomical and other data for various flowering plant groups the development of DNA sequencing technologies which have increasingly been applied to plants, leading to the production of large amounts of DNA sequence data the analysis of these morphological and molecular data by cladistic, phyletic, phenetic and other analytical procedures made possible by the availability of high speed computing capacity the development of electronic databases and information systems, as a result of advanced technology, capable of storing large amounts of data about all aspects of plants Although often referred to as the molecular age of systematics, the current phase of taxonomy and systematics is much wider than just the use of DNA sequence data on their own, and it would be more accurate to refer to it as the phylogenetic (or cladistic) and bioinformatic phase. What is remarkable is the production of large datasets of morphological as well as molecular information and the construction of tree diagrams, most frequently cladograms, from these in various combinations. Indeed the combination of disparate datasets is one of the strengths of today s systematics and classification as well as providing both philosophical and technical challenges. As we comment in the successor to Flowering Plants of the World (Heywood et al. 2007), these phylogenetic analyses have undoubtedly led to a much greater understanding of the evolution of flowering plants and although molecular systematics is still in its early stages, there is general agreement as to the basic framework of a phylogenetic system of classification for the flowering plants. It has led to major realignments of families, the association of families or parts of them not previously regarded as related, the splitting of some families and the merging of others. There is no room for complacency and already remarkable new alignments at the base of the angiosperm tree have been proposed as the result of work on the tiny moss-like aquatic genera Hydatella and Trithuria that comprise the family Hydatellaceae. This was previously thought to belong in the monocots and near the grasses but has now been shown to be closely related to the water-lilies (Nymphaeales), representing a new ancient lineage near the base of the angiosperm evolutionary tree (Saarela et al. 2007). As we bring to bear new approaches in developmental genetics and genomics that will lead to a deeper understanding of the systematics, classification and relationships of the flowering plants, we may expect further modifications to our classifications both at family and lower levels. Phenetic and phylogenetic species At the species level, which for many of us is the frontline of taxonomy, the debate continues to rage about the nature of species, witness for example, the volume by Wheeler and Meier (2000) and the current set of commentaries by Henderson (2005, 2006) and Jensen (2006) in Systematic Botany. I refer also to a paper in Nature in which Rieseberg et al. (2006) conclude that 70 percent of taxonomic species and 75 percent of phenotypic clusters in plants correspond to reproductively independent lineages and therefore represent biologically real entities (begging the question as to what real means!). One could, of course, also conclude from this that traditional taxonomists are doing a good job, despite the criticisms often directed at them! And in The Systematist, Olivier Rieppel (2006) discusses the thesis that species and other taxa are to be considered individuals as opposed to classes or sets which are considered abstract universal concepts. While such arcane debates (cf. Rieppel 2007) are intellectually absorbing and a logical consequence of treating

4 42 Heywood taxonomy and systematics as rigorous academic disciplines (which they are, but not entirely so), one can t help wondering if more effort might not be better directed at devising more effective means of exploring and measuring populations of plants in the field and recognizing the phenetic groups we call species and which Rieseberg tells us are acceptable in most cases. Species have to be used by a wide range of interest groups and as Cracraft (2000) uncompromisingly states: we should be careful in seeking justification for a particular species concept if it cannot embrace the vagaries of real-world data with aplomb. No hemming. No hawing. It must work. This does not mean that we should abandon theory and philosophy, ontology and epistemology, individuality, reality, pattern versus process, and all the other notions that orbit around discussions of species concepts. But we must keep our feet firmly planted on the ground. I personally deplore the near demise of what one used to term biosystematic or experimental taxonomic studies in which the focus was on the nature and dynamics of species populations and their reproductive biology and breeding relationships. Indeed, if we abandon the notion of species as representing essentially dynamic and variable populations of largely interbreeding individuals in nature, however difficult they might be to delimit, then we risk losing much of what makes taxonomy such an absorbing and valuable pursuit. SO WHERE ARE WE NOW? How far the transformation of systematics and in particular molecular analysis has illuminated our understanding of the Compositae is very difficult to answer. Clearly great advances have been made, but with ca. 24,000 30,000 species in over genera (Funk and Robinson 2005; Funk et al. 2005; Hind 2007; Kadereit and Jeffrey 2007) it is not surprising that many problems remain at all levels and in all areas of Compositae research. There seems to be developing something of a convergence of opinion, although by no means unanimity, over the major subdivisions of the family, or at least the recognition of two sister groups, one comprising the monophyletic Barnadesioideae with a single tribe and about 100 species, and the other containing the great bulk of the family comprising a more narrow than previously circumscribed paraphyletic Cichorioideae with some species and the large monophyletic Asteroideae with the remaining 18,000 or so species. Others (see Chapter 11) favor breaking up the paraphyletic Cichorioideae; only time will tell which system works the best. Hind (2007) in his treatment of the family in Flowering Plant Families of the World, echoes Jeffrey s remarks nearly thirty years earlier, that the classification of the family is still in a state of transition and there is no agreement yet on whether to accept monotypic subfamilies or to recognize supersubtribes sensu Jeffrey (2004) or supertribes sensu Robinson (2004). Wagenitz (1976) observed some thirty years ago that it is remarkable that the tribes as created by Cassini in the early 19 th century have not been fundamentally altered, and Per Ola Karis (2006) has recently made a similar comment regarding the Panero and Funk (2002) system, noting how it corresponds strikingly well to the tribal system founded by Cassini almost 200 years ago. The level of sampling of tribes and genera so far achieved in the molecular systematics of Compositae is still very low in many cases despite the impressive achievements of the past two decades, and a great deal of consolidation will be needed before we can feel comfortable with many of the new alignments. Again, although some progress has have been made in our knowledge and understanding of structural and functional aspects of the family, the biology of the capitula, phytochemistry and biochemical pathways, the economic importance of the group, genomic evolution and analysis, and the reproductive biology and conservation status of most of its 25,000 species, there are still enormous gaps in our knowledge. We need to remember that little is known of the majority of species apart from some basic facts of their morphology and location, and their existence as coherent, repeatable population-based phenomena is only suppositional (Heywood 1988: 48). For most of them, their demography, reproductive biology, breeding system, genetic variability and so on is virtually unstudied. Yet the fact is that for many purposes, the users of our classifications require information beyond identification and description of genera and species. They may demand detailed ecogeographic and population data on the species so that effective conservation can be planned. They will need to assess the likelihood of individual species successfully migrating or surviving in the new ecoclimatic envelopes that will develop as a consequence of climate change. Already there have been calls for taxonomists to take into account the needs of conservation in designing Floras and other taxonomic outputs ( Golding and Timberlake 2003; Heywood 2003; Leadlay and Jury 2006), and it is inevitable that taxonomists will be called upon to play a key role in responding to the consequences of global change. As Agapow et al. (2004) point out, the ways in which species are defined is a concern not only of the taxonomist but of the conservation biologist. The consequences of the adoption of different definitions can be serious, for example in the compilation of lists of threatened species and conservation legislation.

5 Chapter 2: The recent history of Compositae systematics 43 LOOKING TO THE FUTURE Looking to the future, what can we expect? One view is that presented in the concluding section of Krupnick and Kress s book on Plant Conservation (Krupnick and Kress 2005), in which they envisage the future age of plant exploration and discovery in the 21 st century. They see image-recognition software, electronic field guides, DNA bar-coding, palmtop and wearable computers, GPS receivers and web-based satellite communication. Field botanists will be able to immediately compare their newly collected plants with type specimens and reference collections archived and digitized in museums thousands of miles away. Information will be gathered and sent back to their colleagues in the laboratory to rapidly determine the genetic composition and phylogenetic position of each new species. While some of these techniques are already available, we need to consider such a scenario in the light of practicalities, cost-effectiveness, and likelihood of implementation. To repeat Cracraft s admonition, we must keep our feet firmly planted on the ground. Although taxonomy currently is riding high on the back of the biodiversity bandwagon on the one hand and the excitement of molecular phylogenetic discovery and explanation on the other, neither is likely to retain their privileged recognition, and I agree with Olmstead (2006) that systematics will then need to reinvent itself yet again if it is to survive as a dynamic academic discipline. In the case of Compositae, at what stage or level of construction of the metatree on the one hand, and exploration and description of new taxa and revision of species-rich and/or critical groups will our paymasters and peers say, enough is enough? Of course, there is another scenario. All the evidence suggests that the combined effects of global change (demographic, disturbance regimes, climatic), combined with unsustainable levels of consumption and use of energy will over the coming decades force dramatic changes on our current models of society and trade. This will impact on all our lives and institutions and lead to a rewriting of our priorities, not to mention research into taxonomy and systematics whether it be of plants, animals, or microorganisms, let alone Compositae systematics. What role taxonomy and systematics will play in such a world will to a large extent depend on our actions now. But until the crunch comes, let us enjoy working with these fascinating plants that give us so much pleasure. Literature cited Agapow, P.M., Bininda-Emonds, O.R.P., Crandall, K.A., Gittleman, J.L., Mace, G.M., Marshall, J.C. & Purvis, A The impact of species concept on biodiversity studies. The Quarterly Review of Biology 79(2): Anderberg, A.A., Baldwin, B.G., Bayer, R.J., Breitwieser, I., Jeffrey, C., Dillon, M.O., Eldenäs, P., Funk, V., Garcia- Jacas, N., Hind, D.J.N., Karis, P.O., Lack, H.W., Nesom, G., Nordenstam, B., Oberprieler, C., Panero, J.L., Puttock, C., Robinson, H., Stuessy, T.F., Susanna, A., Urtubey, E., Vogt, R., Ward, J. & Watson, L.E [2006]. Compositae. Pp in: Kadereit, J.W. & Jeffrey, C. (eds.), The Families and Genera of Vascular Plants, vol. 8, Flowering Plants. Eudicots. Asterales. Springer, Berlin. Bremer, K Asteraceae: Cladistics & Classifi cation. Timber Press, Portland. Caligari, P.D.S & Hind, D.J.N. (eds.) Proceedings of the International Compositae Conference, Kew, 1994, vol. 2, Com positae: Biology and Utilization. Royal Botanic Gardens, Kew. Cracraft, J Species concepts in theoretical and applied biology: a systematic debate with consequences. Pp in: Wheeler, Q.D. & Meier, R. (eds.), Species Concepts and Phylo genetic Theory: A Debate. 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