Contributions to Zoology, 79 (4) – 2010Michel Laurin: The subjective nature of Linnaean categories and its impact in evolutionary biology and biodiversity studies
Biological criteria for rank assignment at a given level

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Imprecision in the meaning of taxonomic names

Given that the absolute rank assignment of taxa is subjective, ranking and delimitation of taxa can vary substantially between authors, or even between papers by a single author. This problem can affect any biological field, because biological knowledge is usually taxon‑specific; more than 1.5 million species have been described, and there are probably between 3.5 and 10.5 million extant species (Alroy, 2002). Thus, most biological knowledge is useful to the extent that the clade to which it applies is known with some precision. No objective reason for changing the rank allocation of a taxon, or for attributing a ranked taxon to another clade than specified in the original study is required by any of the rank‑based codes. Similarly, the rank‑based codes allow taxa to be put into synonymy (Fig. 1b) or for additional taxa to be erected within previously recognized taxa (Fig. 1c, d) without any justification or change in our objective knowledge about nature (i.e. discovery of new species or change in our understanding of the phylogeny). Thus, to take a simple hypothetical example consisting of four species (j-n) forming two genera (O and P) and one family (Oidae) under the originally proposed nomenclature (Fig. 1a), twelve alternative, equally, simultaneously and indefinitely valid nomenclatures can be proposed (Fig. 1b-d), resulting in thirteen nomenclatures. Under that system, the delimitation of taxa is ambiguous; hypothetical genus O can include species j and k, as in the original nomenclature, but it can also include only its type species j (Fig. 1c) or species j-n (Fig. 1b). The delimitation of family Oidae can fluctuate in the same way. The number of possible nomenclatures increases very fast with the number of taxa considered, so this number must be extremely high for the biodiversity that is already known. This problem occurs even in the case in which the phylogeny is stable and in which no new species is discovered, a combination of circumstances that should lead to maximal nomenclatural stability.

Much confusion arose in the discussions of nomenclatural stability in PN and RN because three kinds of nomenclatural stabilities (maximal, minimal, and realized) were conflated. Some proponents of RN have argued that the lack of precision in delimitation in RN is an advantage because it allows the limits of taxa to be adjusted when the phylogeny changes and when new taxa are discovered (Benton, 2007). This argument rests on the untested assumption that systematists spontaneously agree on the name and delimitation of taxa; if this were true, no system of biological nomenclature would be required. This is the maximal nomenclatural stability allowed by the system (Laurin, 2008), and it is undeniably greater than under PN, but it is seldom achieved, as empirical examples provided below demonstrate. The minimal nomenclatural stability provided by a system, if users abide by its rules, is probably more relevant, and it is in this respect that PN vastly outperforms RN because under a given phylogeny, only one delimitation of each taxon is generally possible (Fig. 1e, f). The debates between proponents of RN and PN can thus be reformulated in terms of the relative importance of minimal and maximal nomenclatural stability. Which one should be maximized? Minimal stability should be maximized if taxonomists generally fail to spontaneously agree on taxon delimitation, but maximal stability should be maximized if systematists generally agree on taxon delimitation. To determine which situation prevails, case studies of the realized nomenclatural stability are needed, and a few are provided below. However, various statements in the literature suggest that spontaneous agreement on nomenclatural matters is rare; after all, ‘It has been said that most scientists would rather use another scientist’s toothbrush than his terminology’ (McShea, 2000: 330).

Empirical studies show that the lack of delimitation provided by RN result poor realized nomenclatural stability, although this has been thoroughly investigated for few taxa. For instance, Rowe and Gauthier (1992) showed that the delimitation of Mammalia (ranked as a class, in rank‑based nomenclature) has varied greatly between authors, and even between various studies by a given author (Fig. 3a). The least inclusive clade called ‘Mammalia’ in the literature that they surveyed is usually called Theria (the smallest clade that includes placentals and marsupials), and the most inclusive Synapsida (the largest clade that includes mammals but not extant reptiles). The difference in composition between the least and most inclusive clades thus called Mammalia is modest if only extant forms are included because Monotremata was the only extant taxon that has been excluded by a small minority of studies. However, when extinct forms are considered (Fig. 3b-d), the difference is great, no matter which criterion is emphasized. For instance, the time of origin of the least inclusive clade (Theria) is no earlier than Jurassic according to some molecular dating studies (Bininda‑Emonds et al., 2007), and the paleontological evidence suggests an even later (Early Cretaceous) age of about 130 Ma (Benton and Donoghue, 2007). At the other extreme, Synapsida is known to have originated in the Carboniferous, at least about 315 Ma ago (Marjanović and Laurin, 2007). When looking at the morphology, the diversity of aspects encompassed by the first mammal is also impressive. At one extreme, the first therian was probably a moderately small (less than 25 cm snout‑vent length; Hu et al., 2005), possibly nocturnal, viviparous form with mammary glands and fur (Carroll, 1988). At the other extreme, the first synapsid was probably oviparous, devoid of mammary glands, diurnal, hairless, and larger, with a snout‑vent length of about 34 cm (Laurin, 2004).

FIG2

Fig. 3. Delimitation of the taxon Mammalia under rank‑based (RN) and phylogenetic nomenclature (PN). Under RN, the name Mammalia (a) has been applied to several nested clades (some of which are identified by an asterisk), as shown by Rowe and Gauthier (1992). Under PN, the name could be defined using a crown-, apomorphy-, or total clade definition (numbers 1-3 in bold, blue type), but, once published in conformity with the PhyloCode, one definition would have priority and would not change. Most proponents of PN use a crown‑clade definition of Mammalia (as shown here), but many proponents of RN have advocated using the appearance of the dentary/squamosal joint to delimit Mammalia, although this proposal has not been consistently followed. The possible time of appearance of several other mammalian characters is shown. The vertical bar denotes the considerable uncertainty that surrounds the time of origin of most non‑skeletal ‘mammalian’ characters, which are known in the crown, but whose presence in other members of more inclusive taxa (e.g. Cynodontia, Eutheriodontia, Therapsida) cannot be assessed. A few taxa that have been occasionally considered part of Mammalia under RN are illustrated: Tetraceratops (b), Haptodus (c), and the dinocephalian Titanophoneus (d). Modified from Laurin and Cantino (2007) and Laurin and Reisz (1990). Scale bar (b-d) equals 2 cm. The geological time scale is from Gradstein et al. (2004). The two periods that could not be labeled on the figure because of lack of space are (from bottom to top) the Guadalupian and Luopingian (Middle and Late Permian). Abbreviations: D/Sq J, dentary‑squamosal joint; En, endothermy; Ha, hair; M Gl, mammary glands; Ma, million year ago; Mar, Marsupialia; Mo, Monotremata; Pl, Placentalia.

It could be argued that in the case of Mammalia, rank‑based nomenclature could not stabilize their delimitation only because, under the ICZN, taxa above the family-series have no types. However, two facts refute this argument. Firstly, the ICZN and the ICNB clearly state that rank‑based nomenclature does not delimitate taxa. Thus, according to Principle 2 in the introduction of the ICZN (1999), ‘[n]omenclature does not determine the inclusiveness or exclusiveness of any taxon, nor the rank to be accorded to any assemblage of animals, but, rather, provides the name that is to be used for a taxon whatever taxonomic limits and rank are given to it.’ General Consideration 4 of the ICNB likewise states that ‘[r]ules of nomenclature do not govern the delimitation of taxa…’ (Lapage et al., 1990). Thus, rank‑based nomenclature seems to have been designed specifically to avoid delimiting taxa. This is perplexing because at least some proponents of rank‑based nomenclature suggest that nomenclatural stability ‘would certainly be greatly appreciated by non‑systematists’ (Dubois, 1988: 31). Secondly, problems in delimitation similar to those evoked above for Mammalia also plague lower‑ranking taxa in the family- and genus-series. For instance, Keesey (in Laurin and Bryant, 2009) showed that names typified by Homo or Homo sapiens were associated with two (Hominoidea) to six (Hominidae) nested clades. Similar problems have affected names in the genus Rana (Hillis and Wilcox, 2005; Frost et al., 2006; Dubois, 2007b). In this case, the problem is exacerbated by the low number of Linnaean categories available to describe the diversity of the very speciose genus Rana (over 1000 species). Because of this, Hillis and Wilcox (2005) erected subgenera within subgenera, but, as pointed out by Dubois (2007b), this is contrary to the basic principles of rank‑based nomenclature (although the ICZN, contrary to the ICNB, does not state this clearly). Proponents of rank‑based nomenclature have long recognized that delimitation of taxa under that system is unstable, even at ranks at which taxa have types under the ICZN, such as the genus (Dubois, 1988). This brief review hopefully shows that the subjective nature of Linnaean categories contributes to vagueness in the meaning of taxon names, which is hardly surprising given that the authors of the rank‑based codes apparently think that taxa should be left undelimited.