A review of criticisms of phylogenetic nomenclature: is taxonomic freedom the fundamental issue?

The proposal to implement a phylogenetic nomenclatural system governed by the PhyloCode), in which taxon names are defined by explicit reference to common descent, has met with strong criticism from some proponents of phylogenetic taxonomy (taxonomy based on the principle of common descent in which only clades and species are recognized). We examine these criticisms and find that some of the perceived problems with phylogenetic nomenclature are based on misconceptions, some are equally true of the current rank-based nomenclatural system, and some will be eliminated by implementation of the PhyloCode. Most of the criticisms are related to an overriding concern that, because the meanings of names are associated with phylogenetic pattern which is subject to change, the adoption of phylogenetic nomenclature will lead to increased instability in the content of taxa. This concern is associated with the fact that, despite the widespread adoption of the view that taxa are historical entities that are conceptualized based on ancestry, many taxonomists also conceptualize taxa based on their content. As a result, critics of phylogenetic nomenclature have argued that taxonomists should be free to emend the content of taxa without constraints imposed by nomenclatural decisions. However, in phylogenetic nomenclature the contents of taxa are determined, not by the taxonomist, but by the combination of the phylogenetic definition of the name and a phylogenetic hypothesis. Because the contents of taxa, once their names are defined, can no longer be freely modified by taxonomists, phylogenetic nomenclature is perceived as limiting taxonomic freedom. We argue that the form of taxonomic freedom inherent to phylogenetic nomenclature is appropriate to phylogenetic taxonomy in which taxa are considered historical entities that are discovered through phylogenetic analysis and are not human constructs.     

A logic approach to modelling nomenclatural change

We utilize an Answer Set Programming (ASP) approach to show that the principles of nomenclature are tractable in computational logic. To this end we design a hypothetical, 20 nomenclatural taxon use case, with starting conditions that embody several overarching principles of the International Code of Zoological Nomenclature, including Binomial Nomenclature, Priority, Coordination, Homonymy, Typification and the structural requirement of Gender Agreement. The use case ending conditions are triggered by the reinterpretation of the diagnostic features of one of 12 type specimens anchoring the corresponding species‐level epithets. Permutations of this child‐to‐parent reassignment action lead to 36 alternative scenarios, where each scenario requires a set of 1–14 logically contingent nomenclatural emendations. We show that an ASP transition system approach can correctly infer the Code‐mandated changes for each scenario, and visually output the ending conditions. The results provide a foundation for further developing logic‐based nomenclatural change optimization and validation services, which could be applied in global nomenclatural registries. More generally, logic explorations of nomenclatural and taxonomic change scenarios provide a novel means of assessing design biases inherent in the principles of nomenclature, and can therefore inform the design of future, big data‐compatible identifier systems that recognize and mitigate these constraints.     

Zoological nomenclature in the century of extinctions: priority vs. ‘usage’

Our epoch is a crucial one for scientific knowledge of the organisms that live on our planet. The combination of the biodiversity crisis and the taxonomic gap results in taxonomic urgency. In this context, great attention should be paid to the nomenclatural rules helping taxonomists in their urgent task, rather than diverting their time and energy to secondary questions or debates. In zoology, the new criterion of ‘prevailing usage’, introduced in the 1999 edition of the Code of nomenclature to ‘protect’ some nomina, raises four kinds of problems: (1) it weakens the binding value and strength of the Code, thus indirectly bringing support to the development of alternative nomenclatural systems; (2) it encourages personal debates among taxonomists, giving undue importance to the ‘argument of authority’ in nomenclatural decisions; (3) it sends a wrong message to non-taxonomists as regards completion of the taxonomic work; (4) it acts as a threat against natural history museums, in devaluing onomatophores (type specimens), the conservation of which is one of their major ‘visible’ functions. In conclusion, it is suggested that ‘protection’ of some nomina ‘threatened’ by rules of the Code should be limited strictly to nomina well-known outside the small world of systematics. This would require new rules for the Code to clearly define categories of usage on the basis of objective criteria.     

Prokaryotic taxonomy and nomenclature in the age of big sequence data

The classification of life forms into a hierarchical system (taxonomy) and the application of names to this hierarchy (nomenclature) is at a turning point in microbiology. The unprecedented availability of genome sequences means that a taxonomy can be built upon a comprehensive evolutionary framework, a longstanding goal of taxonomists. However, there is resistance to adopting a single framework to preserve taxonomic freedom, and ever increasing numbers of genomes derived from uncultured prokaryotes threaten to overwhelm current nomenclatural practices, which are based on characterised isolates. The challenge ahead then is to reach a consensus on the taxonomic framework and to adapt and scale the existing nomenclatural code, or create a new code, to systematically incorporate uncultured taxa into the chosen framework.Subject terms: Archaea, Bacteria     

The Linnaean system and its 250-year persistence

The Linnaean system of nomenclature has been used and adapted by biologists over a period of almost 250 years. Under the current system of codes, it is now applied to more than 2 million species of organisms. Inherent in the Linnaean system is the indication of hierarchical relationships. The Linnaean system has been justified primarily on the basis of stability. Stability can be assessed on at least two grounds: the absolute stability of names, irrespective of taxonomic concept; and the stability of names under changing concepts. Recent arguments have invoked conformity to phylogenetic methods as the primary basis for choice of nomenclatural systems, but even here stability of names as they relate to monophyletic groups is stated as the ultimate objective. The idea of absolute stability as the primary justification for nomenclatural methods was wrong from the start. The reasons are several. First, taxa are concepts, no matter the frequency of assertions to the contrary; as such, they are subject to change at all levels and always will be, with the consequence that to some degree the names we use to refer to them will also be subject to change. Second, even if the true nature of all taxa could be agreed upon, the goal would require that we discover them all and correctly recognize them for what they are. Much of biology is far from that goal at the species level and even further for supraspecific taxa. Nomenclature serves as a tool for biology. Absolute stability of taxonomic concepts—and nomenclature—would hinder scientific progress rather than promote it. It can been demonstrated that the scientific goals of systematists are far from achieved. Thus, the goal of absolute nomenclatural stability is illusory and misguided. The primary strength of the Linnaean system is its ability to portray hierarchical relationships; stability is secondary. No single system of nomenclature can ever possess all desirable attributes: i.e., convey information on hierarchical relationships, provide absolute stability in the names portraying those relationships, and provide simplicity and continuity in communicating the identities of the taxa and their relationships. Aside from myriad practical problems involved in its implementation, it must be concluded that “phylogenetic nomenclature” would not provide a more stable and effective system for communicating information on biological classifications than does the Linnaean system.     

Reconciliation of evolution and nomenclature among the higher taxa of protists*

Existing taxonomic schemes for the protists at the highest levels are confusing owing to insensitivity to evolutionary data, lack of stability, evolutionary misleading terminology and multiple, contradictory systems. We propose a system which circumvents these problems by recognizing the largest monophyletic groups possible, and creating a nomenclature for these by appending the suffix ‘protista’ onto an already recognizable prefix: for example, euglenoprotista, cilioprotista, chytridioprotista. This system provides a high degree of stability while also allowing for the further clustering of these groups and inclusion of their descendant groups, such as the plants, as more evolutionary data become available.     

New proposals for naming lower-ranked taxa within the frame of the International Code of Zoological Nomenclature

The recent multiplication of cladistic hypotheses for many zoological groups poses a challenge to zoological nomenclature following the International Code of Zoological Nomenclature: in order to account for these hypotheses, we will need many more ranks than currently allowed in this system, especially in lower taxonomy (around the ranks genus and species). The current Code allows the use of as many ranks as necessary in the family-series of nomina (except above superfamily), but forbids the use of more than a few ranks in the genus and species-series. It is here argued that this limitation has no theoretical background, does not respect the freedom of taxonomic thoughts or actions, and is harmful to zoological taxonomy in two respects at least: (1) it does not allow to express in detail hypothesized cladistic relationships among taxa at lower taxonomic levels (genus and species); (2) it does not allow to point taxonomically to low-level differentiation between populations of the same species, although this would be useful in some cases for conservation biology purposes. It is here proposed to modify the rules of the Code in order to allow use by taxonomists of an indeterminate number of ranks in all nominal-series. Such an 'expanded nomenclatural system' would be highly flexible and likely to be easily adapted to any new finding or hypothesis regarding cladistic relationships between taxa, at genus and species level and below. This system could be useful for phylogeographic analysis and in conservation biology. In zoological nomenclature, whereas robustness of nomina is necessary, the same does not hold for nomenclatural ranks, as the latter are arbitrary and carry no special biological, evolutionary or other information, except concerning the mutual relationships between taxa in the taxonomic hierarchy. Compared to the Phylocode project, the new system is equally unambiguous within the frame of a given taxonomic frame, but it provides more explicit and informative nomina for non-specialist users, and is more economic in terms of number of nomina needed to account for a given hierarchy. These ideas are exemplified by a comparative study of three possible nomenclatures for the taxonomy recently proposed by Hillis and Wilcox (2005) for American frogs traditionally referred to the genus Rana.     

Phylogenetic hypotheses, taxonomic sameness and the reference of taxon names

When scientists use a taxon name like Mammalia, it is important that they talk about the same thing. But, what does it mean to be the same thing in different phylogenetic hypotheses? And, how is taxonomic reference maintained across hypotheses? Here, we discuss the differences between real and hypothetical clades, and how such a distinction relates to the sameness problem. Since hypotheses influence how we perceive things and pursue science, we find it important to have a functioning nomenclatural system for clades as perceived in phylogenetic hypotheses. As a solution to the sameness problem for such clades, we argue that a taxon name does not primarily refer to a single clade that somehow mirror the reality of branches in the tree of life. Instead we suggest that a taxon name refers to a set, or natural kind, of counterfactual and reconstructed clades.     

Revised nomenclature for transposable genetic elements

Transposable DNA elements occur naturally in the genomes of nearly all species of prokaryotes. A proposal for a uniform transposable element nomenclature was published prominently in the 1970s but is not, at present, available online even in abstract form, and many of the newly discovered elements have been named without reference to it. We propose here an updated version of the original nomenclature system for all of the various types of prokaryotic, autonomous, transposable elements excluding insertion sequences, for which a nomenclature system already exists. The use of this inclusive and sequential Tn numbering system for transposable elements, as described here, recognizes the ease of interspecies spread of individual elements, and allows for the naming of mosaic elements containing segments from two or more previously described types of transposons or plasmids. It will guard against any future need to rename elements following changes in bacterial nomenclature which occurs constantly with our increased understanding of bacterial phylogenies and taxonomic groupings. It also takes into account the increasing importance of metagenomic sequencing projects and the continued identification of new mobile elements from unknown hosts.     

Molecular phylogenetics of the Meteoriaceae s. str.: focusing on the genera Meteorium and Papillaria

In order to delimit and understand the evolution of the Meteoriaceae, we provide phylogenetic analyses using the internal transcribed spacer 2 (ITS2) of nuclear ribosomal DNA in combination with two plastid markers, trnL-F and psbT-H. In contrast to the widely used trnL-F region, the psbT-H gene cluster, coding for proteins of photosystem II, has been rarely used to address systematic questions among the different land plant lineages. To overcome the problem of potential ambiguous alignments of non-coding DNA regions, the data were independently analyzed using direct optimization. The comparison and evaluation of the obtained results showed that the inferred cladograms based on the different phylogenetic approaches are very similar, with only minor differences. In combination with morphological characters, generic relationships as well as taxonomic and nomenclatural problems, especially regarding the key genera Meteorium and Papillaria are discussed in detail. New insights into generic relationships of the Meteoriaceae are provided, such as the exclusion of the monospecific southern South American genera Ancistrodes and Cryphaeophilum, which are subsequently transferred to the Hookeriaceae and Cryphaeaceae, respectively. Phylogenetic reconstructions using maximum likelihood as well as parsimony approaches reveal that at the familial level the Meteoriaceae s. l. are polyphyletic, if the formerly recognized "Trachypodaceae" are considered as a separate family. Based on our results we favor the synonym of the Trachypodaceae with the Meteoriaceae.     

Least-inclusive taxonomic unit: a new taxonomic concept for biology

Phylogenetic taxonomy has been introduced as a replacement for the Linnaean system. It differs from traditional nomenclature in defining taxon names with reference to phylogenetic trees and in not employing ranks for supraspecific taxa. However, 'species' are currently kept distinct. Within a system of phylogenetic taxonomy we believe that taxon names should refer to monophyletic groups only and that species should not be recognized as taxa. To distinguish the smallest identified taxa, we here introduce the least-inclusive taxonomic unit (LITU), which are differentiated from more inclusive taxa by initial lower-case letters. LITUs imply nothing absolute about inclusiveness, only that subdivisions are not presently recognized.     

Development of the SeqCode: A proposed nomenclatural code for uncultivated prokaryotes with DNA sequences as type

Over the last fifteen years, genomics has become fully integrated into prokaryotic systematics. The genomes of most type strains have been sequenced, genome sequence similarity is widely used for delineation of species, and phylogenomic methods are commonly used for classification of higher taxonomic ranks. Additionally, environmental genomics has revealed a vast diversity of as-yet-uncultivated taxa. In response to these developments, a new code of nomenclature, the Code of Nomenclature of Prokaryotes Described from Sequence Data (SeqCode), has been developed over the last two years to allow naming of Archaea and Bacteria using DNA sequences as the nomenclatural types. The SeqCode also allows naming of cultured organisms, including fastidious prokaryotes that cannot be deposited into culture collections. Several simplifications relative to the International Code of Nomenclature of Prokaryotes (ICNP) are implemented to make nomenclature more accessible, easier to apply and more readily communicated. By simplifying nomenclature with the goal of a unified classification, inclusive of both cultured and uncultured taxa, the SeqCode will facilitate the naming of taxa in every biome on Earth, encourage the isolation and characterization of as-yet-uncultivated taxa, and promote synergies between the ecological, environmental, physiological, biochemical, and molecular biological disciplines to more fully describe prokaryotes.     

Naming taxa from cladograms: a cautionary tale

The recent publication of a new hypothesis of cladistic relationships among American frogs referred to the genus Rana, accompanied by a new taxonomy and a new nomenclature of this group [Hillis D.M., Wilcox, T.P., 2005. Phylogeny of the New World true frogs (Rana). Molecular Phylogenetics and Evolution 34, 299-314], draws attention to the problems posed by the use of a "double nomenclature", following both the rules of the International Code of Zoological Nomenclature (designated here as "onomatophore-based nomenclature") and the rules of the draft Phylocode (designated here as "definition-based nomenclature"). These two nomenclatural systems, which rely upon widely different theoretical bases, are incompatible, and the latter cannot be viewed as a "modification" of the former. Accordingly, scientific names (nomina) following both systems should be clearly distinguished in scientific publications. Onomatophore-based nomina should continue to be written as they have been for about 250 years, whereas definition-based nomina should be written in a specific way, e.g., Lithobates. The combined use of both nomenclatural systems for the same taxonomy in the same paper requires good knowledge and careful respect of the rules of the Code regarding availability, allocation and validity of nomina. As shown by this example, not doing so may result in various problems, in particular in publishing nomina nuda or in using nomenclatural ranks invalid under the current Code. Attention is drawn to the fact that new nomina published without diagnostic characters are not available under the Code, and that the latter currently forbids the use of more than two ranks (subgenus and "aggregate of species") between the ranks genus and species.     

A synopsis of Goniothalamus species (Annonaceae) in Thailand, with descriptions of three new species

A comprehensive taxonomic revision of Goniothalamus species (Annonaceae) occurring in Thailand is presented for the first time. Twenty-five species are recognized, including three that are described as new to science ( Goniothalamus aurantiacus from South-Western Thailand, Goniothalamus maewongensis from Northern Thailand, and Goniothalamus rongklanus from Northern and North-Eastern Thailand). Several taxonomic and nomenclatural misunderstandings are corrected. The name G. griffithii is shown to be widely misapplied for populations in Northern Thailand, for which the name G. calvicarpus should be applied; 'true' G. griffithii is restricted to South-Western Thailand and Myanmar. In addition, the widely used name G. marcanii is shown to be a synonym of G. tamirensis , and the name G. latestigma , previously regarded as a synonym of G. undulatus , is reinstated. Goniothalamus cheliensis is furthermore newly recorded from Thailand. Most species are restricted to Peninsular Thailand and represent a Malesian floristic component.  © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 156 , 355–384.     

The importance of designating type material for uncultured taxa

Naming of uncultured Bacteria and Archaea is often inconsistent with the International Code of Nomenclature of Prokaryotes. The recent practice of proposing names for higher taxa without designation of lower ranks and nomenclature types is one of the most important inconsistencies that needs to be addressed to avoid nomenclatural instability. The Code requires names of higher taxa up to the rank of class to be derived from the type genus name, with a proposal pending to formalise this requirement for the rank of phylum. Designation of nomenclature types is crucial for providing priority to names and ensures their uniqueness and stability. However, only legitimate names proposed for axenic cultures can be used for this purpose. Candidatus names reserved for taxa lacking cultured representatives may be granted this right if recent proposals to use genome sequences as type material are endorsed, thereby allowing the Code to be fully applied to lineages represented by metagenome-assembled genomes (MAGs) or single amplified genomes (SAGs). Genome quality standards need to be considered to ensure unambiguous assignment of type material. Here, we illustrate the recommended practice by proposing nomenclature type material for four major uncultured prokaryotic lineages based on high-quality MAGs in accordance with the Code.     

On the origin of prokaryotic "species": the taxonomy of halophilic Archaea

The consistent use of the taxonomic system of binomial nomenclature (genus and species) was first popularized by Linnaeus nearly three-hundred years ago to classify mainly plants and animals. His main goal was to give labels that would ensure that biologists could agree on which organism was under investigation. One-hundred fifty years later, Darwin considered the term species as one of convenience and not essentially different from variety. In the modern era, exploration of the world's niches together with advances in genomics have expanded the number of named species to over 1.8 million, including many microorganisms. However, even this large number excludes over 90% of microorganisms that have yet to be cultured or classified. In naming new isolates in the microbial world, the challenge remains the lack of a universally held and evenly applied standard for a species. The definition of species based on the capacity to form fertile offspring is not applicable to microorganisms and 70% DNA-DNA hybridization appears rather crude in light of the many completed genome sequences. The popular phylogenetic marker, 16S rRNA, is tricky for classification since it does not provide multiple characteristics or phenotypes used classically for this purpose. Using most criteria, agreement may usually be found at the genus level, but species level distinctions are problematic. These observations lend credence to the proposal that the species concept is flawed when applied to prokaryotes. In order to address this topic, we have examined the taxonomy of extremely halophilic Archaea, where the order, family, and even a genus designation have become obsolete, and the naming and renaming of certain species has led to much confusion in the scientific community.     

On the temporal inconsistencies of Linnean taxonomic ranks

The inconsistency problem in systematics refers in part to the fact that disparate taxa of identical Linnean rank are not necessarily similar or even readily comparable in any other specifiable biological feature. This shortcoming led to a ‘temporal banding’ proposal in which extant clades associated with particular taxonomic ranks would be standardized according to a universal metric: the absolute time of evolutionary origin. However, one underexplored possibility is that same‐level taxa in disparate organismal groups already might be similar (fortuitously so) in evolutionary age. In the present study, we explicitly address this possibility by reviewing published molecular inferences about the known or suspected origination dates of taxonomic genera, families, and orders in diverse organismal groups. Our findings empirically confirm that currently recognized taxa are far from temporally standardized, thereby adding support for the contention that this kind of taxonomic inconsistency should ultimately be rectified in our biological classifications. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 707–714.