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      Phylogenetic classifications are informative, stable, and pragmatic: the case for monophyletic taxa

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          Abstract

          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.

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          The evolution of myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae)

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            Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches.

            Termites are instantly recognizable mound-builders and house-eaters: their complex social lifestyles have made them incredibly successful throughout the tropics. Although known as 'white ants', they are not ants and their relationships with other insects remain unclear. Our molecular phylogenetic analyses, the most comprehensive yet attempted, show that termites are social cockroaches, no longer meriting being classified as a separate order (Isoptera) from the cockroaches (Blattodea). Instead, we propose that they should be treated as a family (Termitidae) of cockroaches. It is surprising to find that a group of wood-feeding cockroaches has evolved full sociality, as other ecologically dominant fully social insects (e.g. ants, social bees and social wasps) have evolved from solitary predatory wasps.
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              Phylogenomic methods outperform traditional multi-locus approaches in resolving deep evolutionary history: a case study of formicine ants

              Background Ultraconserved elements (UCEs) have been successfully used in phylogenomics for a variety of taxa, but their power in phylogenetic inference has yet to be extensively compared with that of traditional Sanger sequencing data sets. Moreover, UCE data on invertebrates, including insects, are sparse. We compared the phylogenetic informativeness of 959 UCE loci with a multi-locus data set of ten nuclear markers obtained via Sanger sequencing, testing the ability of these two types of data to resolve and date the evolutionary history of the second most species-rich subfamily of ants in the world, the Formicinae. Results Phylogenetic analyses show that UCEs are superior in resolving ancient and shallow relationships in formicine ants, demonstrated by increased node support and a more resolved phylogeny. Phylogenetic informativeness metrics indicate a twofold improvement relative to the 10-gene data matrix generated from the identical set of taxa. We were able to significantly improve formicine classification based on our comprehensive UCE phylogeny. Our divergence age estimations, using both UCE and Sanger data, indicate that crown-group Formicinae are older (104–117 Ma) than previously suggested. Biogeographic analyses infer that the diversification of the subfamily has occurred on all continents with no particular hub of cladogenesis. Conclusions We found UCEs to be far superior to the multi-locus data set in estimating formicine relationships. The early history of the clade remains uncertain due to ancient rapid divergence events that are unresolvable even with our genomic-scale data, although this might be largely an effect of several problematic taxa subtended by long branches. Our comparison of divergence ages from both Sanger and UCE data demonstrates the effectiveness of UCEs for dating analyses. This comparative study highlights both the promise and limitations of UCEs for insect phylogenomics, and will prove useful to the growing number of evolutionary biologists considering the transition from Sanger to next-generation sequencing approaches. Electronic supplementary material The online version of this article (doi:10.1186/s12862-015-0552-5) contains supplementary material, which is available to authorized users.
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                Author and article information

                Contributors
                psward@ucdavis.edu
                Journal
                Insectes Soc
                Insectes Soc
                Insectes Sociaux
                Springer International Publishing (Cham )
                0020-1812
                19 September 2016
                19 September 2016
                2016
                : 63
                : 4
                : 489-492
                Affiliations
                [1 ]Department of Entomology and Nematology, University of California, Davis, CA USA
                [2 ]Department of Entomology, Smithsonian Institution, Washington, DC USA
                [3 ]Department of Entomology, California Academy of Sciences, San Francisco, CA USA
                Article
                516
                10.1007/s00040-016-0516-9
                5052292
                27773940
                e19f7e5d-61a8-40cd-bec4-1309eb0a59b7
                © The Author(s) 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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                © International Union for the Study of Social Insects (IUSSI) 2016

                Entomology
                Entomology

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