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Species Delimitations in Plants: Lessons Learned from Potato Taxonomy by a Practicing Taxonomist

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Species Delimitations in Plants: Lessons Learned from Potato Taxonomy by a Practicing Taxonomist Journal of Systematics JSE and Evolution doi: 10.1111/jse.12203 Review Species delimitations in plants: lessons learned from potato taxonomy by a practicing taxonomist David M. Spooner* U. S. Department of Agriculture, Agricultural Research Service, Vegetable Crops Research Unit, Department of Horticulture, University of Wisconsin, 1575 Linden Drive, Madison, Wisconsin 53706-1590, USA *Author for correspondence. E-mail: [email protected]. Tel.: 1-608-8900309. Fax: 1-608-2624743. Received 22 January 2016; Accepted 11 April 2016; Article first published online 4 May 2016 Abstract Solanum section Petota has been the subject of intensive taxonomic work since the description of the cultivated potato in 1753. In total, there are 494 epithets for wild taxa and 626 epithets for cultivated taxa. Different taxonomists applied various taxonomic philosophies and species concepts to the section. Hypotheses of the number of species and their interrelationships have differed greatly among authors. A taxonomic treatment of section Petota by Jack Hawkes in 1990 recognized 228 wild species and seven cultivated species, divided into 21 taxonomic series. In 2014 Spooner and collaborators more than halved this number to 107 wild species and four cultivated species, partitioned into four clades; not using series. The purpose of this paper is to provide a retrospective of the methods and philosophies that have resulted in this drastic decrease in the number of species and their infrasectional classification. Key words: phylogeny, potato, Solanum section Petota, species. Species Problems and Taxonomic Back- recognized 21 taxonomic series, 228 wild species, and seven ground of Solanum Section Petota cultivated species. Spooner et al. (2014) more than halved this number of As detailed by Spooner & van den Berg (1992a), Solanum species to 107 wild species and four cultivated species, section Petota has been the subject of intensive taxonomic partitioned into three nuclear clades and not using series work since the description of the cultivated potato, (Figs. 2, 3). These taxonomic decisions and treatments of the S. tuberosum (Linnaeus, 1753). In total, there are 494 epithets monophyletic potato, tomato, section Etuberosum (Bukasov for wild taxa and 602 epithets for cultivated taxa, including & Kameraz) A. Child clade are detailed in five monographic names not validly published (Ovchinnikova et al., 2011). treatments: 1) wild potatoes from North and Central America Different taxonomists applied various taxonomic philosophies (Spooner et al., 2004); 2) wild potatoes from southern South to the section, but mainly have used morphology to define America, including close outgroup section Etuberosum species. Hypotheses of the number of species and their (Spooner et al., 2016); 3) the wild potatoes of northern South interrelationships have differed greatly among taxonomists America (Spooner et al., unpublished data); 4) cultivated (Fig. 1). Indeed, the great discordance of taxonomic treat- potatoes (Ovchinnikova et al., 2011); and 5) wild tomatoes ments of section Petota was used as one of the four examples (Peralta et al., 2008). The purpose of this paper is to describe (also including sorghum, maize, and wheat) that stimulated the methods and philosophies that have resulted in this Harlan & de Wet (1971) to abandon traditional taxonomy as of drastic decrease in the number of species and infrasectional any reliable guide to plant breeders and rather to classify classification from series to clades. It freely draws upon germplasm entirely on a biological species concept (their gene information summarized in Spooner (2009, 2011) and Spooner pool concept). The first modern and comprehensive (from et al. (2014) but refocused as a personal retrospective on throughout the entire range of the group) taxonomic addressing species delimitation and their interrelationships. treatment of section Petota was provided by Hawkes I always had intense curiosity about plant names, and (1956), followed by a similar treatment by Correll (1962), learned in my teens how to use Gleason & Cronquist (1963) but with the addition of extensive specimen citations and and various local floras to identify plants in Ohio and adjacent excellent illustrations. This taxonomy was supplemented by states. I used to play “botany at 55 miles an hour” with my significant regional taxonomic treatments by Hawkes & botany friends, where we first identified plants sitting in the Hjerting (1969, southern South America), Hawkes & Hjerting field, and then from afar travelling in a car, using their colors (1989, Bolivia); Ochoa (1990, Bolivia), and Ochoa (1999, Peru). and shapes and habitats. This experience eventually led to a The taxonomic treatment by Hawkes (1990) was the standard job as a field botanist with the Ohio Department of Natural comprehensive treatment for many years, where he Resources where for three years I spent much of five months May 2016 | Volume 54 | Issue 3 | 191–203 © 2016 This article is a U.S. Government work and is in the public domain in the USA. 192 Spooner Fig. 1. A chronological history of the hypotheses of placement of species into series by Correll (1962), Bukasov (1978), Gorbatenko (1989), and Hawkes (1990). The non-italicized names of Bukasov have been treated as series but are not validly published. Solid lines connecting series indicate the maintenance or transfer of species between series. Dotted lines indicate that an author did not treat these series. The numbers in circles are the number of species accepted for the series (from Spooner & van den Berg, 1992a). J. Syst. Evol. 54 (3): 191–203, 2016 www.jse.ac.cn Species delimitations in plants 193 as reproductive isolation, diagnosability, and monophyly, and showing how these various criteria are expected to appear at different times and in different orders in the evolution of different groups of species. New concepts and debates of species continue to arise, such as one arguing that many autopolyploid derivatives of diploid species should be provided separate species status (Soltis et al., 2007). The literature on the reality of species and methods to define them has been so voluminous that Rieseberg & Burke (2001) stated “The discussion of species concepts has become a cottage industry.” Reviews on the history, definition, and concepts of species have summarized fully 22 concepts by Mayden (1997) and 26 by Wilkins (2009). In the modern era with phylogeny as a unifying biological concept, most taxonomists today equate species with lineages. The majority of practicing taxonomists assume, by definition of what we do in investigating species boundaries and writing monographs, that species are “real” in the sense I did when I began my work; that is, we can recognize most to be morphologically coherent and we use a variety of techniques, including ecology, inter- crossability, chromosome numbers, anatomy, DNA, often using multiple genes (e.g., Zang et al., 2011), or any other Fig. 2. A summary cladogram showing relationships among characters, to help discover and define them, that is, using the three nuclear clades of section Petota, similar to the an eclectic approach (e.g., Stuessy, 1990). The clearest plastid relationships but combining species of plastid clades species definition I have read that applies this philosophy is þ into nuclear clade 1 2, and immediate outgroups in the the “phylogenetic species concept” stressing both phylog- tomato clades and section Etuberosum clade, based on the eny and diagnosability (e.g., Cracraft, 1989). In reality, every molecular analyses mentioned in this paper. This is followed group differs in the biological criteria impacting species fi by a comparison of the classi cations of Hawkes (1990) and divergence, setting up a sliding scale from well-defined to Spooner et al. (2004) as a result of these studies, and problematical species. Therefore, the degree of diagnos- additional studies at the species level. ability will vary from group to group, forever maintaining individual taxonomic decisions on species that may vary from taxonomist to taxonomist. Hence, a search for a simple each year in the field searching for rare plants. It became clear “formula” to use any individual criteria, or set of criteria, to that some groups (e.g., Craetegus, Oenothera, Rubus, some define species will forever be an elusive goal. The best species of oaks, and others), were difficult, and I ascribed the taxonomists can do is to state clearly their data sources and intergradation of their component species to hybridization, species philosophy and hopefully those with the best quality apomixis, recent divergence, or some other complex genetic data and analyses will be those who have their taxonomies phenomena. My point, however, is that those with field adopted. Below follows the data and philosophies I have experience can easily note the majority of the species to be encountered in potato. “good”, assuming that morphological divergence is a valid proxy for good species. When I entered graduate school this simplistic view of Biological Factors Complicating the species was modified as I was exposed to the vast and often Solanum Petota contentious literature debating what constitutes species, Systematics of Section ranging from some (Ehrlich & Raven, 1969; Levin, 1979) Wild and cultivated potatoes have long plagued taxonomists arguing that gene flow is too limited among conspecific plant into constructing an easy and repeatable taxonomy address- populations to allow species to evolve as evolutionary units ing the resolution
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