In a recent commentary in this journal Seifert et al. (2016) propose returning to
a school of classification largely abandoned by systematists, in which both monophyletic
and paraphyletic groups are formally recognized. This approach, dubbed “evolutionary
classification”, has proved to be unattractive and impractical because the basis for
taxon recognition is a confounding mix of phylogenetic relatedness and some measure
of “degree of divergence”. Most systematists and evolutionary biologists now advocate
classifications that are strictly phylogenetic, in which all named taxa above the
species level are monophyletic (Wiley and Lieberman 2011; Vences et al. 2013; Judd
et al. 2016). Hence, in contemporary biology textbooks birds are acknowledged to be
part of the reptile clade; non-monophyletic groups such as “Pisces” and “Articulata”
have been abandoned; and a primary division of flowering plants into “dicots” and
monocots is recognized as untenable (Westheide and Rieger 2013, 2015; Freeman et al.
2014; Sadava et al. 2014; Judd et al. 2016). In entomology, paraphyletic groups such
as “Homoptera”, “Heterocera”, and “Apterygota” are no longer part of insect classification
(Gullan and Cranston 2014; Beutel et al. 2014). Others, such as Blattodea, have been
redefined to encompass all their descendant taxa, and hence avoid paraphyly—in this
case by including termites in the cockroach order (Inward et al. 2007). Of course,
vernacular terms exist for some paraphyletic assemblages (moths, algae, fish, invertebrates,
etc.), but most of them are no longer treated as formal groups in a classification.
One could argue that scientific controversies should not be decided by majority rule
alone, but there are sound reasons why biological systematists overwhelmingly favor
a phylogenetic classification. Such a scheme is simply more informative, accurate,
and predictive. Birds really are a kind of modified reptile; to place them in a different
group, separate from reptiles, obscures this important fact. Similarly, inclusion
of termites in the order Blattodea emphasizes that they are indeed “social cockroaches”
and this leads to a more insightful understanding of their biology and evolution (Bell
et al. 2007). Excluding termites from Blattodea and putting them in their own order,
Isoptera, would be positively misleading.
A phylogenetic classification is also, ultimately, more stable: as we refine our understanding
of the tree of life, and achieve ever more confident estimates of phylogenetic relationships,
systematists are more likely to converge upon a consensus. In a phylogenetic classification
not all nodes in the tree of life need to be named, but any group that is named must
meet the criterion of monophyly, and this limits the number of available options (Schmidt-Lebuhn
2012). By contrast, allowing paraphyletic groups opens up a can of worms. How distinct
does a divergent ingroup have to be to justify excising it from its containing group
and thereby render the latter paraphyletic? Given that rates of evolution are highly
variable, and also vary among different classes of characters, there would be no end
of argument—never resolved satisfactorily—about whether a given group is “sufficiently
distinct” to be removed from its containing clade.
Consider the examples to which Seifert et al. (2016) objected. In our recent reclassification
of the ant subfamily Myrmicinae (Ward et al. 2015), we placed lineages of socially
parasitic ants into the genera in which they are embedded phylogenetically. Although
these parasites had been placed in their own genera on the basis of their divergent
phenotypes, our molecular phylogenetic results demonstrated that they are nested within
more inclusive genera such as Tetramorium and Temnothorax, which each contain hundreds
of species. Ongoing molecular studies show that the social parasites are situated
shallowly within their respective host genera (F. Hita Garcia, pers. comm.; M. Prebus,
pers. comm.), precluding a simple splitting into several monophyletic subgroups.
Moreover, contrary to the claim by Seifert et al. (2016) that the social parasites
have diverged markedly while other congeners have remained more or less phenotypically
static, there is a broad range of variability among the other species. For example,
Temnothorax ants have undergone an impressive radiation in the Caribbean, producing
species that are, at least superficially, far more divergent morphologically from
typical Holarctic species of Temnothorax than the social parasites (Fig. 1). But there
are varying degrees of extremeness in these Antillean Temnothorax (Fontenla 2000).
Where along this range of variation should a break be made? Then there is the erstwhile
subgenus Dichothorax, also well embedded in Temnothorax, with unusual mesosomal morphology.
Should it be removed too? What about the pale nocturnal Temnothorax that have diversified
in the deserts of Baja California? Or the Mesoamerican radiation of the Temnothorax
salvini group? Depending on the whim and subjective perceptions of different “evolutionary
systematists”, various parts of Temnothorax could be amputated, leaving behind an
ill-defined assortment of species, scattered across the phylogeny.
Fig. 1
Morphological diversity in workers of the ant genus Temnothorax. a
T. ravouxi (CASENT0173641), a social parasite formerly known as Myrmoxenus ravouxi,
b
T. unifasciatus (CASENT0173188), the most commonly used host species of T. ravouxi,
c
T. pergandei (CASENT0104016), formerly in subgenus Dichothorax, d
T. salvini (CASENT0010847), part of a Mesoamerican radiation of the genus, e
T. bca05 (CASENT0118165), a member of a species complex occurring in the deserts of
Baja California, f
T. poeyi (CASENT0106241), an extreme representative of the Caribbean radiation of
Temnothorax.
Images from AntWeb (http://www.antweb.org)
No matter how such an operation is performed, it would always result in a loss of
information content for Temnothorax. Under a phylogenetic classification, Temnothorax
contains all members that share a most recent common ancestor. Under any paraphyletic
formulation, this does not hold true. The increased efficiency of information retrieval
that a phylogenetic system produces has been recognized in the literature for some
time (Cracraft 1974; Farris 1979; see also Schmidt-Lebuhn 2013).
The argument that communication is hindered by adoption of a phylogenetic classification
also does not stand up to scrutiny. The former parasite genera can be referred to
using informal species-group names. For a period of time one could append the old
genus name, e.g., “ravouxi-group (former Myrmoxenus)”, until usage of the species-group
name takes over. There are numerous examples among ants of other satellite genera
that were previously synonymized under their containing clades: Doronomyrmex under
Leptothorax; Sifolinia under Myrmica; Anergatides, Bruchomyrma, Sympheidole and others
under Pheidole; various former genera under Strumigenys, etc. No-one is any longer
decrying the loss of these genus names; the species names (or informal species-group
names) are still available and permit ready communication about the taxa concerned.
It is ironic that Seifert et al. (2016) exhort the reader to consider the experience
of plant systematists. In fact, there have been major advances in the systematics
of flowering plants, as botanists have developed a revised phylogenetic classification
that incorporates the findings from molecular studies (Stevens 2016). The Angiosperm
Phylogeny Group (APG) project is an excellent example of how the Linnaean system can
be modified to accommodate new phylogenetic knowledge and to reflect relatedness (Angiosperm
Phylogeny Group 2016). Seifert et al. (2016) fail to mention the APG initiative; instead
they cite two botanists whose views (e.g., Stuessy & Hörandl 2014) are at variance
with those of most plant systematists (cf. Kadereit et al. 2016).
Of course there can be challenges to the establishment of a ranked phylogenetic classification—in
principle, for example, when dealing with putatively ancestral taxa (Schmidt-Lebuhn
2012), and in practice when faced with variable rates of morphological evolution among
extant species (Ward 2011), and differing opinions about taxon circumscription and
diagnosability (Christenhusz et al. 2015). The APG classification has undergone multiple
iterations and is still the subject of ongoing discussion—motivated in part by new
phylogenetic information, or by lingering uncertainties about relationships—but thanks
to the unifying principle of phylogenetic relatedness a measure of consensus has been
achieved that is difficult to imagine under the alternative of an “evolutionary classification”.
We are at an exciting time in the study of ants and other social insects where molecular
data—increasingly at the genome scale (e.g., Blaimer et al. 2015)—is yielding unprecedented
insight into their evolutionary history. Indeed, the whole-genome scans of socially
parasitic ants and their hosts advocated by Seifert et al. (2016) have already commenced
(e.g., in Pogonomyrmex and Vollenhovia; Smith et al. 2015), guided by the same phylogenetic
context that also supports the classification of these social parasites in the same
genera as their hosts. The advent of robust molecular phylogenies presents an opportunity
to revise the taxonomy of social insects in line with new findings, and thereby establish
a more stable and informative classification. The call by Seifert et al. (2016) to
return to an outdated classification scheme would reverse this progress, and it should
not be heeded.