Comparative studies that rely on supraspecific taxa
Using rank‑based nomenclature can lead to various problems that concern especially evolutionary biology. These include placing unnecessary constraints on the taxonomic sample and placing undue confidence in absolute or relative biodiversity indices derived from counts of higher taxa, an approach called taxonomic surrogacy. The first problem can occur when taxa of a given rank are selected to trace the evolution of a character. For instance, Smith et al. (2009: fig. 3) inferred the evolution of the cecal appendix in mammals using 79 taxa ranked as families, in addition to Amphibian and Reptilia (usually ranked as classes). While the use of taxa of a given rank (families) gives the reassuring appearance of a homogeneous sampling effort, this was probably not the best strategy because the appendix evolved much faster in some taxa than in others. Thus, in Laurasiatheria, a major clade of placental mammals that probably originated near the K/T boundary (about 65 Ma ago), the appendix never appeared. In Euarchontoglires (another large clade of placentals originating near the K/T boundary), the appendix evolved so fast that inferring its evolution using character optimization is difficult. In several of the ‘families’, the appendix was scored as ‘variable’ (usually termed ‘polymorphic’) when only some species in the taxon had an appendix (Smith et al., 2009: 1992). A more accurate estimate of the character history would have been obtained by replacing the polymorphic terminal taxa by smaller clades (typically ranked as genera) showing a single state. Thus, in this case, use of Linnaean categories gave unjustified confidence in a suboptimal taxonomic sampling scheme.
The problems raised by taxon surrogacy are even more acute. Prance (1994) showed that the neotropical region has a much greater biodiversity of embryophytes than equivalently sized paleotropical regions at the species level (Table 1). Looking at biodiversity at the genus or family level suggests that the flora of Africa and Malesia is about as diverse as that of the neotropics. It might be tempting to accept the conclusion that the neotropics support a greater biodiversity than the paleotropics based on Prance’s (1994) data, but this may not be justified. Perhaps systematists working in the neotropics were just more extreme ‘splitters’ when erecting species (or they may have erected a greater proportion of subjective synonyms) than those working in the paleotropics. Conversely, perhaps botanists working in the paleotropics preferred to include fewer species in each genus and family than botanists working in the neotropics, a question that has long divided systematists (Dubois, 1988); in this case, the neotropics might really have a greater biodiversity than the paleotropics. Another possibility is that the neotropics are home to a greater proportion of geologically recent species, which would explain that the number of genera and families is no higher in the neotropics than in the paleotropics. If Linnaean categories approximately reflected geological time, the three levels (species, genus, and family) would tell us something about the biodiversity of paleo- and neotropics. Unfortunately, this correlation, if present at all, seems to be very weak (Laurin, 2005; Bertrand et al., 2006), and rank assignment of taxa is too subjective to be informative. Bertrand et al. (2006: table 1) provided a compelling example of this using annelids.
Table 1. Biodiversity of embryophytes of the Neotropics and Paleotropics. Modified from Prance (1994).
Other studies have also found that using taxa of a given category to predict the biodiversity at a lower taxonomic level is problematic. For instance, Andersen (1995) showed that the number of ant genera in Australian localities was rather poorly correlated (r2 ≅ 0.5) with the number of species, and that the regression coefficient varied between habitats, size of area surveyed, and sampling effort, thus complicating the use of genus count to predict species counts. Grelle (2002) reported a fairly good correlation between the number of species and that of genera of neotropical mammals (r2 = 0.8) in various localities, but this varied strongly between taxa. Explained variance ranged from 0.45 for rodents to 0.96 for primates. Family and order number were generally not significantly correlated with species numbers. These patterns largely reflect the number of species per genus, family, and order, in taxonomies and in localities. As Grelle (2002) suggested, genus richness is often a good predictor of species richness when most genera are represented by one or two species in each locality. As that number increases, precision of the estimate of species number decreases. Thus, Terlizzi et al. (2003: 558) noted that ‘[t]he response of different taxonomic levels might change according to biogeographical features and internal diversity of taxa’; thus, ‘if the family richness is a good surrogate of species diversity in the North Sea, it might not be the same for the Mediterranean sea’. This conclusion is confirmed by the subjective nature of Linnaean categories, but the very fact that studies are still done on the efficiency of taxon surrogacy suggests that the subjective nature of absolute ranks is not fully understood by many biologists. Terlizzi et al. (2003: 559) concluded that taxonomic surrogacy ‘may be tolerated only when difficulties in sampling, data analysis and identification of some particular organisms make this procedure strictly necessary, not merely to save costs whatever the aim of the study is’, and appropriately noted that ‘[i]f species loss is the main concern of conservation biology (together with habitat loss), it is simply absurd to pretend to perform conservation studies without considering species.’
The lack of unified concepts of individual Linnaean categories precludes interpretation of patterns found through taxon surrogacy. For instance, Grelle (2002: 105) reported that, in most neotropical localities, primates and marsupials were generally represented by a single species in each genus (but several genera per locality); in contrast, several species of bats and rodents represented each genus. Grelle (2002) suggested that these differences reflected a higher turnover of primate and marsupial species than of bats and rodents. This is not likely because bats (1100 species) and rodents (2277 species) are the most speciose clades of placental mammals (5400 species, approximately; species counts from Wilson and Reeder, 2005), and since their antiquity is approximately equal with that of primates and less than that of marsupials (Wible et al., 2007), the diversification rate of bats and rodents has obviously been higher than that of most other mammalian clades (marsupials and primates have about 334 and between 190 and 350 species, respectively). Similarly, Grelle’s (2002: 105) suggestion that the difference in pattern between primates and marsupials on one hand, and rodents and chiropterans on the other, reflects ‘different assembly rules organizing (or not) these communities’ is not fully warranted. Such an interpretation might possibly be validated if it were shown that the minimal divergence time between primate or marsupial species co‑occurring in localities were significantly different from that of rodent or chiropteran species that co‑occur in similar localities. An alternative interpretation would be that ecological divergence allowing habitat sharing occurs faster in some of these taxa than in others. But such conclusions must rest on time‑calibrated trees, not on ‘ontologically empty’ (Ereshefsky, 2002: S309) Linnaean categories.
Even the species level is not completely objective in the absence of a universally agreed‑upon and universally applied species concept, and Ereshefsky (2002) has forcefully argued that this Linnaean category is as subjective as any other, even among sexually reproducing organisms. Furthermore, the equivalence between species of sexually reproducing organisms and asexual ones is even more problematic (Turelli et al., 2001: 336). Pleijel and Rouse (2003) even argued that we should drop the term ‘species’ and use the more ontologically neutral term LITU (least inclusive taxonomic unit) instead to denote the smallest recognizable clades. Thus, it could be argued that even counting species is not adequate to assess biodiversity, and that more objective indices based on phylogenies and evolutionary time should be used, such as Faith’s (1992) phylogenetic diversity index (PDI). The PDI is simply the sum of branch lengths linking all terminal taxa (of an area, or a clade, or of any group of taxa of interest). Computing the PDI is now feasible for many taxa since user‑friendly software such as Mesquite (Maddison and Maddison, 2009) can compute it, at least with some optional modules (Josse et al., 2006). The only remaining difficulty is obtaining a phylogeny of the relevant taxa with estimated divergence times, but recent progress in molecular (Thorne and Kishino, 2002; Sanderson, 2003; Brochu, 2004) and paleontological dating (Marjanović and Laurin, 2007, 2008) should facilitate this in the future. This is already shown by large compilations of time‑calibrated trees (e.g. Hedges and Kumar, 2009). Studying floral biodiversity of the paleo- and neotropics using the PDI would allow testing of the various hypotheses formulated above to explain the apparently greater biodiversity of the neotropics than the paleotropics.
All this raises serious questions about the validity of long‑admitted biodiversity patterns shown by paleontological and neontological examples. Many classical paleontological studies about the evolution of biodiversity through the Phanerozoic have been done at the family (e.g. Raup, 1979; Raup and Sepkoski, 1984) or genus level (Raup and Boyajian, 1988). Bertrand et al. (2006: 150) reviewed several such studies and pointed out that the most comprehensive paleontological databases that have been used to study the evolution of biodiversity are still compiled at the genus or family level. Various neontological studies about diversification have assessed dominance (the proportion of taxa at a given rank present in a single taxon of a higher rank, among a taxon of a still higher rank) and have argued that the ‘hollow curve distribution’ (HCD) implies that ‘one clade (or several clades) has had many more speciation events and/or fewer extinctions than other clades at the same taxonomic level’ (Dial and Marzluff, 1989: 26). That would be interesting (it would translate into a higher diversification rate) if taxa of a given rank were monophyletic and had equal geological ages, but neither is required by rank‑based nomenclature, and neither is true in the vast majority of taxonomies. Even though monophyly is increasingly enforced by authors and the lack of monophyly of taxa has been described as one of the greatest limitations of the use of taxonomies to assess biodiversity (Gaston and Williams, 1993: 5), some authors still claim that monophyly should not be required (e.g. Stuessy and König, 2008), and the commissions responsible for emending the rank‑based codes refuse to enforce monophyly as a taxonomic requirement (Laurin, 2008: 224). Yet, the adverse effects of using paraphyletic taxa were clearly shown, among other examples by Patterson and Smith (1987), in the context of assessing cyclicity in extinction patterns. Until dominance and HCD are reassessed on clades of equal geological age (regardless of absolute rank), the significance of these patterns will remain unknown.