Planning the future of plant systematics: Report on a special colloquium at the Royal Netherlands Academy of Arts and Sciences

Forty botanists from 13 countries met this March in Amsterdam at a special colloquium at the Royal Netherlands Academy of Arts and Sciences to discuss the future of plant systematics (“Beyond the Tree of Life: the Future of Plant Systematics”; Fig. 1). The meeting was funded by the Netherlands Royal Academy and organized by Erik Smets (Naturalis Biodiversity Center, Leiden, Netherlands) and colleagues*; it addressed several paradoxes in our field. First, with an ongoing planetary-scale biodiversity crisis, the need for plant systematists has never been greater, and yet taxonomic expertise appears to be in steady decline, as noted by repeated calls for action (e.g., de Carvalho et al., 2007; Drew, 2011). Despite this, new plant species are continuously being discovered, and plant systematics as a field has survived and even thrived, thanks to the common overarching goal of building and understanding the Tree of Life, spurred by the availability of new technology and powerful analytical frameworks. Yet, members of the public and colleagues outside biology often express surprise when new plant species are discovered or appear unaware that the Tree of Life is far from being fully resolved. In this context, how do we justify the importance of continued research on plant biodiversity and explain its importance to the general public, university administrators, funding agencies, and policy makers? The organizers identified three central questions for the colloquium to help address these issues: (1) What are the big questions for plant systematics? (2) How should we train the next generation of systematists? (3) How can we emphasize the prominent role of systematics to the outside world, to safeguard the future of our field? Group photograph of the colloquium participants, taken on the third day at the Trippenhuis in Amsterdam. From left to right, top to bottom: Chelsea Specht, Lars Chatrou, Timo van der Niet, Leni Duistermaat, Pedro Crous, Peter Linder, Vincent Merckx, Tod Stuessy, Eric Schranz, Wouter Los, Frederic Lens, Alexandre Antonelli, Niels Raes, Sandra Knapp, Marc Sosef, Pieter Baas, Jorinde Nuytinck, Karol Marhold, Sean Graham, Hans ter Steege, Paul Hoekstra, Muthama Muasya, Mike Thiv, Nina Rønsted, Erik Smets, Michelle Price, Hervé Sauquet, Saroj Ruchisansakun, James Byng. The structure of the meeting and the breadth of attendees were well suited to addressing these questions. Participants represented multiple branches of systematics, including descriptive taxonomy, morphology, phylogenetics, ecology, mycology, genomics, biodiversity informatics, and medicinal botany, and spanned the full range of career stages (from graduate students to senior professors) and diverse institutions (including universities and natural history museums). They came mostly from Europe (around half from the Netherlands), and included representatives from Asia, Canada, South Africa, and the United States. In the morning and early afternoon of each day, a small number of speakers gave short (half hour) talks on a broad diversity of relevant topics, ranging from work on contemporary floras and monographs, to next-generation phylogenetics and emerging computational tools for biodiversity informatics (Table 1). In addition, short shotgun sessions were included that gave all participants the chance to give flash talks or express opinions on topics of interest, and brainstorming discussion sessions concluded each day. Erik Smets started off the meeting by explaining the need for the colloquium. He argued that a critical problem is that society has a poor understanding of the relevance of plant systematics, in part because many people mistakenly think that we already know everything there is to know about plants. A key challenge for the future will thus be to bridge the gap between society and our science, to explain to humanity why it is important to address what we do not know yet about plant diversity, in all its guises. We outline here the major ideas that emerged from the invited talks and summarize conclusions from the discussion sessions. As we hope to demonstrate, this was a highly fruitful, interactive and enjoyable colloquium and a welcome opportunity to reflect on a field at a critical time of transformation. While it is important to acknowledge that the field has continuously changed and that introspection about and planning for the future of systematics has occurred on several occasions in the past (Ehrendorfer, 1970; Stevens, 2000; Sytsma and Pires, 2001), several of the challenges discussed during this meeting represent important new developments, in particular those related to new tools and methods, and to new forms of teaching and communication. Several speakers presented examples on the recent history of our field and how new approaches are transforming research. For example, Marcel Dicke (Wageningen University, Netherlands) introduced the concept of the phytobiome (macrobiome plus microbiome) of plants, and presented a large project on natural variation and biotic interactions of Arabidopsis thaliana. Pedro Crous (CBS Fungal Biodiversity Centre, Utrecht, Netherlands) presented work on fungal pathogens of plants, showing how specimen-level molecular phylogenies of fungal pathogens have become critical for trade control and human health, where traditional systematic approaches have largely failed. Alexandre Antonelli (University of Gothenburg, Sweden) reviewed the current state and future prospects for building and synthesizing the Tree of Life, using phylogenomic and new bioinformatic tools. Tod Stuessy (Ohio State University, Columbus, OH, USA) documented the history of classification principles. Concerning our knowledge about plant species, Peter Linder (University of Zurich, Switzerland) reviewed the history of species concepts to emphasize that describing and naming species had been one of the greatest enterprises ever undertaken by humanity. He presented species as a true “can of worms” and argued that we needed to start understanding the “worms” much better, by studying patterns of inheritance, gene flow, and selection. Mike Thiv (Natural History Museum, Stuttgart, Germany) argued for the need to link species concepts with next-generation sequencing (NGS) and epigenetic data, and insisted that facilitating feedback from plant systematics to conservation will be essential for preserving biodiversity. Timo van der Niet (University of KwaZulu-Natal, Durban, South Africa) reviewed current understanding of speciation processes, about which many unknowns remain, including understanding species and populations in contexts beyond relationships in the Tree of Life. Muthama Muasya (University of Cape Town, South Africa) noted that Africa represents an urgent gap in plant systematics, as the continent is home to 45,000 flowering plant species representing four major biogeographic regions. Although fundamental plant biodiversity research is not yet a funding priority in most African countries, a bright spot is that DNA barcoding has been embraced as a means of blending traditional and molecular approaches to documenting plant diversity. Genome-focused approaches hold the potential to revolutionize our understanding of the plant tree of life and plant biology. Sean Graham (University of British Columbia, Vancouver, BC, Canada) reviewed the use of NGS data in plant phylogenetics. Specifically, he showed how data from plastid genomes (e.g., Ross et al., 2016) and transcriptomes (1KP or One Thousand Plants initiative; Wickett et al., 2014) are already contributing to improving our understanding of higher-order plant phylogeny. He also pointed to exciting emerging NGS phylogenetic initiatives such as the PAFTOL (Plant and Fungal Trees of Life; http://science.kew.org/strategic-output/plant-and-fungal-trees-life) project at the Royal Botanic Gardens, Kew and GoFlag (http://flagellateplants.group.ufl.edu/), an NSF/Genealogy of Life funded project aiming to sequence all “flagellate plant” species (nonflowering land plants, including several lineages with nonflagellate sperm). Citing a recent example from the backbone of fern phylogeny (Rothfels et al., 2015), he pointed out that phylogenomic studies may end up refining rather than revolutionizing our understanding of plant relationships. Chelsea Specht (University of California, Berkeley, CA, USA) highlighted results from an ongoing study using targeted exon capture that successfully resolved relationships in Zingiberales, when whole plastid genomes turned out to be insufficient. She also presented ARBOR, a new platform to facilitate diverse comparative analyses based on the idea of customized and publishable workflows, including innovative data visualization tools currently under development (Harmon et al., 2013). Another example of a new tool was provided by Rutger Vos (Naturalis Biodiversity Center), who described SUPERSMART (Self-Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa), a new pipeline for building and dating phylogenetic trees using GenBank data for any given clade or set of species (Antonelli et al., 2016). How do we train the next generation of plant systematists in increasingly competitive funding environments? Hervé Sauquet (Université Paris-Sud, France) presented a project for an Innovative Training Network (ITN) proposal submitted to the European Commission to prepare the next generation of botanists for service to society both in and outside academia through high-quality international training of 15 Ph.D. students. He explained how developing this proposed program with 10 other European laboratories led to a very fruitful reflection on the skill set and tool kits required for training “next-generation” botanists, which convinced him that sharing knowledge and passion about plant science with the general public is a critical communication skill that we all need to work on. The latter was illustrated in particular by the Massive Open Online Course (MOOC) on introductory botany created by the French association Tela Botanica (http://mooc.tela-botanica.org/), an associated partner in the ITN proposal. The MOOC (in French) has attracted more than 33,000 participants, demonstrating strong interest and demand from the general public in botany training opportunities. New teaching tools and approaches were also discussed with respect to undergraduates and the broader public. James Byng (Naturalis Biodiversity Center) presented the activities of The Flowering Plant Gateway, a nonprofit organization that teaches botanical courses and produces synthetic books at a time when some countries (such as the UK) have nearly abandoned student training in plant sciences (http://www.telegraph.co.uk/news/science/steve-jones/8001565/Where-have-all-the-British-botanists-gone-just-when-we-need-them.html). He argued, “We need more botanical bibles!” As a means of connecting plant systematics to a broader public, Nina Rønsted (University of Copenhagen, Denmark) explained how collections and plant systematics are important resources for improving human health, using examples from her work on medicinal plants. She presented a 2-minute snapshot of a future movie (“The Quest for Cinchona—A Phylogenetic Tale”) on a recent field trip in Bolivia to be used as a new case study for teachers and schools. Our community has an unfortunate tendency to lament the perception of systematics by the public and colleagues from other scientific disciplines. Alexandre Antonelli invited us to “stop complaining and do fantastic things!” He pleaded for the development of policy for the use of public databases in systematics, noting “If it's not in a database, it doesn't exist.” Concerning how systematists work, Sandy Knapp (Natural History Museum, London, UK) pointed that there is a mistaken perception that taxonomists/systematists work alone, in contrast to fields like physics where scientists are perceived to work in very large groups on ambitious projects. Increasingly, however, plant systematics is a massively collective endeavor, exemplified by large collaborative projects like The Plant List (http://www.theplantlist.org/), which build on several long-running databases including Tropicos (http://www.tropicos.org/) and the International Plant Names Index (http://www.ipni.org/). She also noted that, despite common complaints by taxonomists, it is also not necessarily the case that taxonomic papers are more poorly cited than other biological papers (Steiner et al., 2015), a concern so long as citation indices drive tenure and funding agencies. She also argued that finding ways to accelerate taxonomic discovery is an essential goal for our future, given that taxonomic capacity to describe species has stagnated in the past few decades (Bebber et al., 2014). Current informatics infrastructure such as JStor Global Plants, GBIF, and the Biodiversity Heritage Library are increasingly important tools to speed up the rate of species discovery and synthesis, but more could be done in this regard. In particular, making all biodiversity data open and freely available is an essential target. Field collections will continue to be central to plant systematic research. Knapp noted that we need to collect more, even in supposedly well-collected regions, and should clear up museum backlogs. However, she noted that the map of scientific collaboration looks quite colonial and warned against “helicopter science” or “science safaris” as the main means of improving knowledge of plant diversity outside the West. Indeed, a key problem in the field is that biodiversity experts are unevenly distributed across the planet. Muthama Muasya highlighted that of ∼2000 botanical collectors in South Africa, only 1% are black Africans. Exemplifying this, existing African floras have mostly been written outside Africa and have often not been updated, and existing botanical collections were once rooted in colonial ideals and mentality. Future priorities if resources continue to be limited may include revising priority genera and tapping into the power of citizen scientists. Continuing the theme of documenting plant diversity, Marc Sosef (National Botanic Garden, Meise, Belgium) pointed out, “We know an awful lot about awfully few species.” He reminded us that the first objective of the Global Strategy for Plant was to plant diversity and that the first of this was the of The Plant List in the means for its continued are The next challenge is to an of all by However, we are very far from meeting this floras and are being by countries on often with of The Online was created to address this but has not yet a major funding to infrastructure and Karol Academy of presented a for the future of botanical monographs, which need to be more with and with other than have been et al., Michelle et de de Switzerland) presented the of the of European an organization that she currently She the need for a new in which the the which critical in developing countries to for and to taxonomic She also presented the of and by to biodiversity in and of in the of the new et al., Wouter (University of Netherlands), of the concluded with an of the infrastructure needed to the research from data capture and to data and He argued that existing initiatives than half of this and that can be in transforming how data are currently being and in biodiversity it to be how this can be A of the colloquium was to discussion sessions addressing general that emerged from the morning to in a transforming world, critical for the future of plant Participants into groups each afternoon for brainstorming sessions that the which the full in a broader The four were by the participants during at the end of the first day. was a but it was as a key in the A general emerged that we need to out the key questions in plant systematics and for the Another important that emerged is how to the field more We also to what plant systematics special with systematics in The first discussion on ways to and taxonomic of future We for building taxonomic and biodiversity at all of the from to Innovative ideas included the of biodiversity for of natural to and the often training and and limited time of teachers in natural ideas to taxonomic at and a strong on outside to the natural through and came as a of taxonomic expertise institutions and countries was as key for preserving knowledge and at the graduate and participants also came up with the idea of collections in natural history as the and associated people to the of taxonomic knowledge and expertise as much as the for existing knowledge included continued of and open to research including and in with existing databases and Our discussion theme us to think outside the and on and ideas to the future of plant biodiversity and that a strong was the of a next-generation that could help current and future botanists the most of and field In to current and data (including and our from the systematic of including systematic of in a of the of We of a new infrastructure that of data (including and to a public with to and once and in infrastructure could be used as a platform for all of and facilitating and species and in such and infrastructure are in major natural history institutions and funding could by making use the of field and in and it may or decades such highly field data funded by public it to a public Future to the next-generation one day, include of and and We also discussed the potential that collective to a of plant biodiversity science as and exciting for broader Several of us have already started to use and to with other and the general public (e.g., Sauquet, collective field not only be for scientific research (e.g., et al., and biodiversity but could also have an on society if by communication initiatives plant biodiversity and understanding of critical conservation and and to a and of plant interest in our field from new these it will be essential that communication become more on from countries and more on and biodiversity The third discussion at questions and that plant systematists as a community may in the key questions (1) How is plant life and how is diversity distributed in time and (2) What are the (3) How many species are and what do we know about How do we the for training and systematists in the developing address these we that a international project at in public the and from each of species range and could and major of funding and and new questions. collaborative projects already for genomes of Fungal and plant transcriptomes However, these projects do not yet the or or the variation of the species, important to be by future major initiatives for understanding the and of plant biodiversity on tools identified to work these represented highlighted the colloquium. They included the need to train the next generation of botanists and to international and projects in plant biodiversity the critical to and databases all of plant and for funding and international and capacity Our discussion on how to communication with the general public and policy Several First, most of us that we should all be much more and more in sharing knowledge and passion for plant research in all forms of is clear that the public is about new species as from the to the recent of et al., and et al., 2016). examples on the and of natural history and the from The a recent science and with a botanical can to public interest and can be for the to the that new plant species are being discovered the of colleagues who are already very in sharing plant on such as Sandy Knapp, and both of this to open an on the platform during the colloquium. Several of us to start a new under are very have the potential to a to the very The started by the of our communication and in a we also came up with the idea of a for plant systematists to with communication and colleagues with communication to and the on and understanding of our by In we all that we needed to be more and how to and to the general public. As a we that and systematics are that most poorly and that, may a mistaken of a science for policy and even colleagues from other scientific disciplines. We start plant biodiversity experts when we to the general public, or even Plant systematists need to to work and train new of plant systematists more than we do at Global plant biodiversity databases are for plant and data sharing are Plant systematists need to more and about our research with the general public. biodiversity science” may be a to as a for current and future The the organizers of the colloquium for all of the participants to this They also acknowledge the Royal Netherlands Academy of Arts and Sciences for funding this The for to this meeting Erik Smets, Frederic Lens, and Vincent and provided on a of this

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