Pitcher Plants (Sarracenia) Provide a 21st-Century Perspective on Infraspecific Ranks and Interspecific Hybrids: A Modest Proposal for Appropriate Recognition and Usage

—The taxonomic use of infraspecific ranks (subspecies, variety, subvariety, form, and subform), and the formal recognition of interspecific hybrid taxa, is permitted by the International Code of Nomenclature for algae, fungi, and plants. However, considerable confusion regarding the biological and systematic merits is caused by current practice in the use of infraspecific ranks, which obscures the meaningful variability on which natural selection operates, and by the formal recognition of those interspecific hybrids that lack the potential for inter-lineage gene flow. These issues also may have pragmatic and legal consequences, especially regarding the legal delimitation and management of Threatened and Endangered Species. A detailed comparison of three contemporary floras highlights the degree to which infraspecific and interspecific variation are treated inconsistently. An in-depth analysis of taxonomy of the North American flowering plant genus Sarracenia (Sarraceniaceae) provides an ideal case study illustrating the confusion that can arise from inconsistent and apparently arbitrary designation of infraspecific ranks and hybrid taxa. To alleviate these problems, we propose the abandonment of infraspecific ranks of “variety” and “form”, and discourage naming of sterile interspecific hybrids except for use in the horticultural or agronomic trade. Our recommendations for taxonomic practice are in accord with the objectives proposed in the Systematics Agenda 2000, Systematics Agenda 2020, and the Global Strategy for Plant Conservation.

the very first task of a true statesman is to rectify the names." From The Analects of Confucius, tr. Simon Leys (1997) Systematists have long struggled with the appropriate designation of infraspecific taxa (subspecies (subsp.), variety (var.), subvarieties (subvar.), form (forma), and subforms) and interspecific hybrids (e.g., Hamilton and Reichard 1992;Stebbins 1993;McDade 1995). The botanical literature is replete with such designations, as early botanists and taxonomists, including Linnaeus, were influenced by the concept of Special Creation and sought to catalog the seemingly infinite range of phenotypic diversity found in nature (Reveal and Pringle 1993). This tendency has been particularly prevalent in the horticultural and agronomic literature, due in part to the economic incentive for providing a range of commercial offerings with desirable traits for ornamental or practical use (see also Hetterscheid and Brandenburg 1995). The generation of interspecific hybrids also has long been a common practice in agronomy (Kingsbury 2009); modern agribusiness often takes advantage of the infertility of vigorously growing hybrids (e.g., proprietary strains of F 1 hybrid maize) to ensure a reliable supply of customers from year-to-year (e.g., Sonka 2001). Darwin's (1859) observation that natural selection acts on infraspecific variation brought a new cognitive perspective to evolutionary biology and systematics that is well reflected in A. M.  contemporary approaches to phylogenetic analysis and evolutionary systematics (e.g., Bateman 2011). Many taxonomists, however, continue to treat infraspecific taxa and interspecific hybrids in ways that fail to account for ongoing dynamics that are continually occurring in the field.
Although new DNA sequencing techniques are identifying genetic variability at increasingly finer scales, these differences may not reflect infraspecific distinctions. Rather, such genetic variation may better be viewed as the historical fragmentation and coalescence of genotypic possibilities that Maddison (1997) summarized in his concept of a phylogeny as a model of the change of interbreeding probabilities through time (a "cloud of gene histories").
Even though the International Code of Nomenclature (ICN) for algae, fungi, and plants continues to recognize the validity of infraspecific ranks, there remains little consensus how or when to distinguish infraspecific taxa from true species. Stebbins (1993: 240) proposed a pluralistic consensus: "[i]n local floras, some authors recognize as separate species, sympatric populations that in many regions keep distinct from each other but that elsewhere form localized hybrid swarms. Other authors designate them as 'varieties.'" But Stebbins' (1993) consensus leads to inconsistent taxonomy. A single entity (i.e., a species, a subspecies, or a hybrid) should be the same thing wherever it occurs. It cannot logically be a species in one location, for example, and a subspecies in another.
On the other hand, the suggestion of a strictly phylogenetic nomenclature consisting of a formal, albeit rank-free, classification system with named but unranked uninomials (Mishler 1999), continues to be fraught by debates over the special status of species relative to other taxonomic ranks (summarized in Cellinese et al. 2012). Systems of phylogenetic nomenclature with named but unranked uninomials conflate the discrete goal of nomenclature (communication about taxa among individuals in a variety of scientific disciplines; Schuh 2003Valleau 2004 A. M.  with the two goals of systematics: taxonomic recognition of species (i.e., using understanding of variation to produce a falsifiable system of classification ;Mayr 1992;Gaston and Mound 1993) and the identification of their hypothesized phylogenetic relationships (see also Wortley et al. 2002).
A third alternative to classical nomenclatural codes and phylocodes was suggested by de Queiroz (2007), who built on Mayr's biological species concept. de Queiroz (2007) suggested that a species can be geometrically represented as a line (lineage) consisting of a continuous series of connected (often overlapping) points. Information transfer (i.e., genotypes) proceeds through time from ancestor (e.g., parent) to descendent (e.g., offspring). A species exhibits persistence through time, for which the duration is greater than a single generation of a representative individual. A sterile or otherwise non-self-sustaining hybrid, in contrast, can be represented as a point, because ancestor-descendent information transfer is not possible. The temporal duration of a sterile hybrid equals its generational time. A parental species and a sterile hybrid resulting from inter-lineage gene flow are not evolutionarily equivalent, and, in our opinion, the latter deserves less recognition than reproductive species because it does not have the potential for persistent transfer of genetic information. Sterile hybrids may be commercially successful, but they are better viewed from a systematic perspective as short-lived interconnections within Maddison's (1997) cloud of gene histories within a given lineage.
Our focus here is on assessing the nature and utility of infraspecific ranks and naming of sterile hybrids. We first build upon work by Hamilton and Reichard (1992) and McDade (1995), and examine the use of infraspecific ranks and hybrids in several classic and contemporary North American regional floristic treatments. We then explore in more detail the confusion generated by the proliferation of infraspecific designations through a case study of the genus Sarracenia Linnaeus (Sarraceniaceae), the Western Hemisphere pitcher plants. Our analysis and case study reinforce several recommendations previously articulated by other systematists and evolutionary biologists, but also provide additional considerations based on our experiences working with this group of plants, which exhibits marked levels of local phenotypic variation that has been recognized taxonomically.  1976). Although the ICN also allows the designation of subvariety and subform, we did not analyze these rarely-used ranks, but our discussion similarly applies to these cases. The use of infraspecific ranks varies among users and treatments; Stebbins (1993) notes that it is inconsistent even in "standard" manuals. For example, for 31 flowering plant genera found in the northeastern U. S. A. and Canada, Fernald (1950), Gleason and Cronquist (1991), and Haines (2011) differ considerably in their recognition and use of infraspecific taxa (Table 2, in which we adjust the number of infraspecific and hybrid taxa for the total number of taxa recognized in each of these floras to account for their different geographic coverage). At one extreme, Fernald (1950) recognized 32% of the total flora as infraspecific taxa. At the other, Haines (2011) recognized only 16% of the taxa as such. This supports previous observations that more geographically limited floras tend to recognize less variability within a taxon (i.e., overestimate endemism because the range of variability across the entire species range is not recognized in regional floras), while underestimating synonymy (Mabberley 1991;Scotland and Wortley 2003). However, 15% of Haines' (2011) flora was considered to be hybrids, whereas only 11% and 7% of Fernald's (1950) and Gleason and Cronquist's (1991) floras, respectively, were hybrids. All three floras recognize varieties, Fernald (1970) and Haines (2011) recognize subspecies, but only Fernald (1970) recognizes forms. Gleason and Cronquist (1991) were more likely to confer species rank than either Haines (2011) or Fernald (1970, whereas Haines (2011) was more likely to identify regional subspecies. In the most recent floras (e.g., NYBG 1972NYBG -2012Flora of North America Editorial Committee 1993-present;Haines 2011;Baldwin et al. 2012), there is consistent recognition of subspecies, varieties, and hybrids, all of which are accorded full taxonomic status (Baldwin et al. 2012), but forms are no longer used ( Table 1).

Infraspecific Ranks and Hybrids in Past and
The proliferation of many infraspecific names and the persistence of named hybrid taxa under different taxonomic ranks in the botanical literature of the early 20 th century (Table 1) correspond with the lack of an enforced uniform Code of Nomenclature prior to 1930 (although the first attempt at a uniform code occurred nearly 75 years earlier: see de Candolle [1867]).
Presently, Division II, Chapter III, Article 24 of the Melbourne Code (McNeill et al. 2012) provides clear structures for the proper naming of infraspecific taxa, such as subsp., var., and forma. Article H3 and Recommendation H3A in Appendix I provide guidelines for the proper naming of hybrid taxa (but see Hetterscheid and Brandenburg 1995). In contrast, the International Code of Zoological Nomenclature (ICZN 2012) does not provide for formal recognition of infrasubspecific groups, but subspecies are considered acceptable as part of a "species group" (Chapter 10, Article 45; ICZN 2012). In the ICZN, subspecies normally are written as trinomials.
All nomenclatural codes facilitate the naming process but none dictate what information should be included in a taxonomic description or flora (but see Article 38.2 of the Melbourne Code, especially Ex. 4, regarding diagnoses). Because the current rate of extinction is rising sharply (Leakey and Lewin 1995), some have argued that it is critical to assign names and ranks to as many undescribed taxa as possible (e.g., Hopkins and Freckleton 2002;Mace 2004;Dobson 2005;Kim and Byrne 2006;Scheffers et al. 2012;Costello et al. 2013). However, the effort to rapidly assign names tends to ride roughshod over the fact that species designations are falsifiable hypotheses (Gaston and Mound 1993) and may artificially inflate the true number of species (Scotland and Wortley 2003). Further, as noted by Bateman (2011) and Tripp and Hoagland (2013), rapid description often precludes inclusion of detailed morphologic, genetic, or phylogenetic information, thus making it difficult to test the hypothesis that a new entity described from only a small number of herbarium specimens is, in fact, a defensible new taxon.
Thus, we gently suggest that botanists be more circumspect in identifying infraspecific taxa and that the requirements for recognition of a new species be more stringent. We elaborate on these ideas using a case-study of a small genus we know well: the North American pitcher plants in the genus Sarracenia (e.g., Naczi et al. 1999;Ellison 2001;Ellison et al. 2004Ellison et al. , 2012Dahlem and Naczi 2006;Ellison and Gotelli 2009;Oswald et al. 2011). (Fig. 1) offers an ideal case study illustrating the taxonomic confusion that affects researchers studying the ecology, evolution, and natural history of the genus as well as regulatory agencies charged with protecting endangered Sarracenia species. The two most current treatments of the genuspublished within 18 months of each other-disagree in many respects (Table 3). The review by Mellichamp and Case (2009) in Flora North America recognizes only 17 non-hybrid taxa: 11 species, plus two subspecies each of S. alabamensis, S. purpurea, and S. rubra. In contrast, McPherson and Schnell (2011) recognize 49 non-hybrid taxa: eight species, six subspecies, 24 varieties, and 11 forms (Table 3). How has this great disparity in taxonomic recognition arisen?

Sarracenia: A Case Study-The carnivorous plant genus Sarracenia
In the first full treatise on carnivorous plants (Darwin 1875), there is scant detail on pitcher plants (not only Sarracenia, but also the two other genera in the family-Darlingtonia and Heliamphora, as well as the unrelated Asian Nepenthes and the Australian Cephalotus).
However, by the end of the 19 th century, Sarracenia was of broad interest in England and across Europe, where amateur botanists and horticulturalists were hard at work propagating, cultivating, and crossing species (Veitch 1906;Macfarlane 1908). Indeed, since the late 1800s, the production and propagation of hybrid individuals has spurred considerable horticultural interest in these plants (Moore 1874;Masters 1881;Veitch 1906 (MacFarlane 1908;Harper 1918;Small 1933). Wherry (1935) included S. jonesii Wherry in his review of the genus, but reassessments and revisionary treatments by Bell (1949) and McDaniel (1971) Among these early systematic treatments, the recognition of infraspecific taxa was relatively uncommon. Macfarlane (1908) recognized no subspecies or forms, but did recognize seven varieties of S. flava differentiated by leaf size and color, and one variety of S. purpurea-A. M.  var. heterophylla, recognized by its complete lack of red pigmentation (now known to be caused by a single-locus mutation: Sheridan and Mills 1998). The only infraspecific taxon recognized by Harper (1918) Maddison's (1997) "historical genetic potentiality," we note that Mellichamp and Case (2009) consider S. purpurea subsp. venosa var. montana simply to be S. purpurea subsp. venosa at the southwest edge of its geographic range. Further research is needed to determine if this taxon should be recognized as a unique subspecies or a fertile hybrid.
Although systematic treatments of the entire genus emphasize species and hybrids while de-emphasizing infraspecific taxa, regional treatments (e.g., Fernald 1970;Radford et al. 1968;Gleason and Cronquist 1991;Haines 2011), field guides (e.g., Sorrie 2011), and general reviews aimed at hobbyists and horticulturalists (e.g., Schnell 2002;McPherson 2007;McPherson and Schnell 2011) continue to identify-and even formally describe-infraspecific taxa (Small [1933] is a notable exception to this rule). Although a handful of subspecies and varieties are geographic isolates, the vast majority of infraspecific taxa are based on variation in a single phenotypic trait, most frequently, leaf color (Table 5). In fact, all 11 forms recognized by McPherson and Schnell (2011) are color-morphs characterized by the lack of production of anthocynanins (Sheridan and Mills 1999). Students of Sarracenia have long noted little systematic value of color (Bell 1949), and even McPherson and Schnell's treatment illustrates a wide range of variability in colors within varieties defined by color. Evidence from allozyme and sequence data also repeatedly demonstrates a lack of clear differentiation among recognized infraspecific taxa (Bayer et al. 1996;Godt and Hamrick 1996, 1999Neyland and Merchant 2006;Ellison et al. 2012). At the other extreme, Zellmer et al. (2012) used pyrosequence data to show that morphologically similar populations of S. alata on either side of the Mississippi River have been reproductively isolated for ~60,000 generations. However, Zellmer et al. (2012) did not proceed to describe the eastern and western populations as subspecies or varieties.
As in many plant taxa, interspecific hybridization is also common in Sarracenia ( Figure   2), and names for many hybrid taxa have been published (Table 4). Many of these remain contested and most lack types (Bell 1952;Nelson 1986). Hybridization in the genus is not surprising, however, because most Sarracenia species diverged from one another < 3 million years ago, likely due to late Neogene, and especially more recent Pleistocene glaciation (Ellison et al. 2012). Hybrid swarms are common in the field, and molecular markers are being developed that may help to better identify hybrids and their parents (Rogers et al. 2010), and to assess the fertility of Sarracenia hybrids.
This inconsistent nomenclature-i.e., "lumping" in peer-reviewed articles and national floras, "splitting" in regional floras, field guides, and popular works (cf. Mabberley 1991;Scotland and Wortley 2003)-continues to plague the taxonomy of Sarracenia (see reviews in Reveal 1993;Ellison 2001;Mellichamp and Case 2009). Ecologists, physiologists, conservation biologists, and others whose work depends on stable and reliable taxonomy, but who usually have insufficient background to distinguish among divergent taxonomic treatments, often have no easy way to decide which taxon they are studying (of course, this problem extends to numerous taxa besides Sarracenia).
But this is not simply an academic problem; as suggested by the epigraph, this instability presents difficulties for managing the rare and endangered taxa of Sarracenia that often inhabit  Hamilton and Reichard (1992), in their survey of a four-year sample of taxonomic monographs, revisions, and notes from 26 journals regarding ferns, gymnosperms, and flowering plants, determined that the use of infraspecific taxa "...is healthy and viable in the eyes of many taxonomists." The ranks of subsp. and var. were the most widely employed infraspecific categories, with little consistency or agreement in their circumscription or taxonomic application among the surveyed taxonomic works. They also noted a strong regional or international bias toward certain categories, possibly reflective of historical perspectives. Similarly, McDade (1995) reported that the most common infraspecific categories in botanical monographs were subspecies and variety, but that the use of "form" had declined through time.
We identified a similarly wide usage of subspecies and varieties, but little use of forms, in northeastern North American floras (Table 2). However, many practitioners use the terms "subspecies" and "variety" interchangeably (McDade 1995), leading to confusion and inconsistent use of these designations across groups. We, along with Hamilton and Reichard A. M. Ellison et al. -14 (1992) and McDade (1995), continue to see a lack of a proper circumscription of the particular use of the rank "subspecies" by most plant taxonomists and systematists. This omission is also an issue in zoological taxonomy and nomenclature (Braby et al. 2012). We thus conclude that, absent the adoption of a uninomial phylocode (e.g., Cellinese et al. 2012) that applies to species and infraspecific taxa, there is a need for uniformity in usage of terms denoting infraspecific taxa that consist of biologically (i.e., evolutionarily) meaningful and distinctive, but incompletely differentiated, groups of lineage-specific individuals.
There has been, over time, an evolution of thought regarding the appropriate use of infraspecific taxonomic categories. A number of treatises on the art and science of taxonomy and systematics have ranged from a simple listing of the hierarchy of infraspecific categories (e.g., Davis and Heywood 1973;Radford et al. 1974;Simpson, 2006) to a comprehensive discussion of the history and biology of these categories (e.g., Stuessy 2009). Following from these, we propose that botanists adopt a (modified) concept of subspecies suggested by Braby et al. (2012; our modifications in italics): "Subspecies comprise evolving populations that represent partially isolated lineages of a well-defined species that are either allopatric or sympatric, phenotypically distinct, have at least one fixed diagnosable character state, and that these character differences are, or are assumed to be, correlated with at least partial evolutionary independence according to population genetic structure." A. M.  At the same time, we strongly discourage continued use of varieties and forms (as well as the allowed, albeit rarely used, subvarieties and subforms). Our conclusion is mirrored in the more recent general trend we identified to deemphasize, or outright discourage, the use of ranks lower than subspecies. As Stuessy (2009: 154) noted, "the usage of subspecies, variety, and form has changed over the years, which has confounded attempts to use the concepts in a consistent fashion." Stuessy (2009) did support the use of both subspecies and varieties in those cases where such designations have proven useful in specific groups, but states "[o]ne suggestion toward uniformity would be to set a future start date, e.g., the year 2011, for the use of only one infraspecific category (preferably the subspecies)," which is the approach used in the most recent and comprehensive treatment of Sarracenia (Mellichamp and Case, 2009). This advice has parallels elsewhere. Among zoologists, Simpson stated that "[o]ne of the commonest and most abused terms in taxonomy has been variety" (Simpson 1961: 177; italics in the original). Simpson also discounted the use of the category "form" and averred (1961: 180) that "[i]n present classification, however, the only acceptable infraspecific category [i.e., rank] is the subspecies." In fact, the current ICZN states that "[n]ames published after 1960 with the term "variety" or "form" [are] excluded" and are not regulated by the Code (ICZN 2012, Article

15.2).
On Hybrids-In the cases where two fertile species, over time, give rise either through hybridization or introgression to demonstrably self-sustaining (e.g., sexually fertile, apomictic, etc.) offspring that constitute a distinctive lineage, then formal naming of the hybrid lineage as a new species would be warranted because it exhibits the same geometric and logical properties as a fertile species (e.g., persistence through generational time, transfer of genetic information). We note that determination of the sterility or fertility of a hybrid taxon is rarely possible from herbarium specimens. Rather, field observations and other supporting information would be needed for conclusive demonstration of fertility. We recognize that obtaining such information can take time, but we suggest that improved taxonomic clarity is well worth the effort (e.g. , Mayr 1992;Helgen et al. 2013). The key to fulfilling any of the goals and objectives of the Systematics Agendas or GSPC is an hypothesis-driven (Gaston and Mound 1993), predictive classification system (Bateman 2011) and the ability to clearly communicate and apply this knowledge to science and society (Daly et al. 2012). We maintain that the proliferation and propagation of names for sterile, nonself-sustaining hybrids and infraspecific names below the subspecies rank does little to shed A. M.  insight into the evolutionary processes at work in said lineages. Furthermore, inconsistent taxonomy and nomenclature adds confusion and inhibits proper and effective communication regarding the true nature of the taxa involved, including in many cases, their conservation, protection, and preservation. A consistent, evolutionarily-based taxonomic system is also needed to ensure that burgeoning citizen-science initiatives aimed at documenting patterns of biodiversity and their rapid changes provide consistent and accurate data (e.g., Hochachka et al. 2012).

Evolution as an Organizing
Recommendations-We offer the following recommendations (some having been stated by previous authors as cited below). 1) For new descriptions of infraspecific taxa, we encourage the single term "subspecies" as the sole infraspecific designation below the rank of species. This term should be applied to a group of individuals only in cases where there is strong supporting evidence of incomplete differentiation, distinct geographic distribution, at least one clearly fixed phenotypic difference, or genetic differentiation that confers the possible evolutionary potential for speciation to occur (e.g., de Queiroz 2007).
2) The use of the infraspecific designations of "form" and "variety" should be abandoned in plant taxonomy and systematics. The International Code of Zoological Nomenclature (ICZN 2012) disallows the use of such categories, and there has been a historical decline in botanical systematics in the use of the category of "form" (Table 1) and the rank of "variety" (e.g., Table 2). In terms of describing or elucidating the nature of the evolutionary process, neither of these terms is of scientific value, and their continued usage only promotes confusion.
A. M.  3) For those groups in which the infraspecific rank "variety" has been used in the past, we suggest that revisionary treatments should encompass infrasubspecific variation in descriptions of species or subspecies. Following Stuessy (2009), we also strongly discourage elevating a "variety" to a "subspecies," unless there is sufficient scientific evidence to warrant such an elevation. Varieties, forms, and other infraspecific ranks should be included in accounts of synonymy since it is crucial to provide continuity with earlier taxonomic treatments. 4) Only self-sustaining (e.g., through sexual reproduction, apomixis, etc.) populations of interspecific hybrids should be provided with formal taxonomic names. Sterile hybrids that arise through occasional syngamy from two distinct species should not be named.
The ability of different species to form sterile hybrids could be noted in their written descriptions. Because it is difficult to determine from herbarium specimens whether a hybrid taxon can form a self-sustaining population, field observations and other supporting information should be sought to support (or reject) formal taxonomic or nomenclatural recognition.
5) The use and retention of "variety" and "form" (as well as "cultivar" or "cultivated variety" and infertile hybrids) should be allowed only for horticultural, agricultural, and ornamental purposes. These terms should only be used to designate desirable phenotypes that have been artificially selected for their practical (i.e., human) use or direct economic benefit, both of which need a clear communication system that reflects commercially desirable phenotypes (see also Hetterscheid and Brandenburg 1995).
ACKNOWLEDGEMENTS-Our work on pitcher plants has been supported most recently by NSF grants 0541680 and 1144056 (to AME); NSF grant 1208835 (to CCD); and an EPSCoR award (to PJC). Elizabeth Farnsworth provided a helpful critique of this manuscript.