Evaluating support for the current classification of eukaryotic diversity

Abstract

Perspectives on the classification of eukaryotic diversity have changed rapidly in recent years, as the four eukaryotic groups within the five-kingdom classification--plants, animals, fungi, and protists--have been transformed through numerous permutations into the current system of six "supergroups." The intent of the supergroup classification system is to unite microbial and macroscopic eukaryotes based on phylogenetic inference. This supergroup approach is increasing in popularity in the literature and is appearing in introductory biology textbooks. We evaluate the stability and support for the current six-supergroup classification of eukaryotes based on molecular genealogies. We assess three aspects of each supergroup: (1) the stability of its taxonomy, (2) the support for monophyly (single evolutionary origin) in molecular analyses targeting a supergroup, and (3) the support for monophyly when a supergroup is included as an out-group in phylogenetic studies targeting other taxa. Our analysis demonstrates that supergroup taxonomies are unstable and that support for groups varies tremendously, indicating that the current classification scheme of eukaryotes is likely premature. We highlight several trends contributing to the instability and discuss the requirements for establishing robust clades within the eukaryotic tree of life.

Figure 1. Trends in the Taxonomy of Eukaryotes

A comparison of four representative taxonomies illustrates trends within eukaryotic taxonomy over the past 50 years [,–7]. Movement of taxa is traced from earlier to more recent taxonomies with solid and dashed lines. A solid line indicates all members of a group (left of line) are incorporated into the subsequent group (right of line). Dashed lines indicate that a subset of members (left) is incorporated into subsequent groups (right).

Figure 2. Summary of Eukaryotic Supergroups

Assessment based on our analysis of molecular genealogies. +++, well supported; +, some support; −, support missing or very limited. Nuclear, genealogies based on nuclear genes. Plastid, genealogies based on chloroplast genes. Pictured organisms: Lesquereusia, Thalassionema, Jakoba, Proterospongia, Cosmarium, Ammonia. (Images: micro*scope, http://starcentral.mbl.edu/microscope).

Figure 3. Trends in Supergroup Taxonomy

A comparison of three formal classifications illustrates trends within (A) “Amoebozoa” [7,45,47]; (B) “Excavata” [7,33,60]; (C) “Plantae” [2,6,7]; and (D) “Rhizaria” [6,7,33]. A majority of solid, horizontal lines would indicate temporal stability of supergroup classification. For visual simplicity we do not indicate groups newly included in the supergroups or taxonomic restructuring within subgroups. Asterisk indicates a newly introduced term. “Chromalveolata” and “Opisthokonta” are not included because only one formal taxonomy exists for both groups. See Figure 1 for further notes.

Figure 4. Support for Membership and Supergroup Monophyly from “Amoebozoa”-Targeted Molecular Genealogies

Membership: • indicates the member taxon falls within the supergroup Amoebozoa; ○ indicates that the member taxon is excluded from the Amoebozoa clade, or no clade is formed. Papers below blank line survey eukaryotic diversity [33,49,115] and are included in all analyses. Member taxa: My, Mycetozoa; Dc, Dictyosteliids; Tu, Tubulinea (Lobosea, Gymnamoebea sensu stricto); Am, Acanthamoebidae; Fl, Flabellinea (Discosea, Glycostylea); Pe, Pelomyxa; Ma, Mastigamoebidae; En, Entamoebidae; Rs, residua; Br, Breviata, “Mastigamoeba invertans sensu NCBI.” Supergroup Monophyly, + indicates monophyly; − indicates group is para- or polyphyletic, and blank indicates insufficient data available. Supergroup definition based on Adl et al. 2005 [4]: A, Amoebozoa; C, Chromalveolata; E, Excavata; O, Opisthokonta; P, Plantae; R, Rhizaria. The position of Breviata, Br, was not considered when scoring the monophyly of Amoebozoa as this organism was misidentified and affiliations are unknown (see text). Some nodes were constrained in reference [97]. References cited in this figure are [25,33,45,48,49,84,97,114,115].

Figure 5. Support for Membership and Supergroup Monophyly from “Chromalveolata”-Targeted Molecular Genealogies

Member taxa: Al, Alveolata; St, Stramenopiles (Heterokonts); Ha, Haptophyta; Cr, Cryptophyceae. Monophyletic “Plantae” from plastid genealogies includes secondarily derived plastids. See Figure 4 for further notes. References cited in this figure are [,,,,,,–122]. Loc, location (genome) from which the gene of interest originated; Pla, plastid genome; Nuc, nuclear genome; Mit, mitochondrial genome.

Figure 6. Support for Membership and Supergroup Monophyly from “Excavata”-Targeted Molecular Genealogies

Member taxa: Di, Diplomonadida; Rt, Retortamonadida; Cp, Carpediemonas; Tr, Trimastix; Ox, Oxymonadida; Ht, Heterolobosea; Eu, Euglenozoa; Ml, Malawimonas; Jk, Jakobida; Pa, Parabasalia; Dy, Diphylleia. Hypothesized subgroups: Fornicata clade (Di + Rt + Cp) monophyletic, Preaxostyla clade (Ox + Tr) monophyletic, ♦ Discicristata clade (Ht + Eu) monophyletic. The position of Diphylleia, Dy, was not considered when scoring the monophyly of “Excavata” as the inclusion of this organism within “Excavata” is controversial and has been removed from recent classifications (see text). See Figure 4 for further notes. References cited in this figure are [,,,,,–128].

Figure 7. Support for Membership and Supergroup Monophyly from “Opisthokonta”-Targeted Molecular Genealogies

Member taxa: Mt, Metazoa; Fu, Fungi; Cf, Choanomonada; Cy, chytrids; Ic, Ichthyosporea (DRIPs); Cl, Corallochytrium; Nu, Nucleariida; Mi, Ministeria; Ap, apusomonads. The position of apusomonads, Ap, was not considered when scoring the monophyly of “Opisthokonta” as this organism is highly variable, and it has been removed from recent classifications (see text). See Figure 4 for further notes. References cited in this figure are [–,,,,,–132].

Figure 8. Support for Membership and Supergroup Monophyly from “Plantae”-Targeted Molecular Genealogies

Member taxa: Gr, Chloroplastida = Viridiplantae (Green algae, including land plants); Rd, Rhodophyceae (Red algae); Gl, Glaucophyta. See Figure 4 for general notes and Figure 5 for plastid-specific notes. References cited in this figure are [,,,,,–139].

Figure 9. Support for Membership and Supergroup Monophyly from “Rhizaria”-Targeted Molecular Genealogies

Member taxa: Ce, Cercomonadida; Ch, Chlorarachniophyta; Eg, euglyphids; Pt, Phytomyxea (plasmophorids); Ph, Phaeodarea; Gr, Gromia; Fo, Foraminifera; Hs, Haplosporidia (Ascetosporea); Po, Polycystinea; Ac, Acantharia; Ds, desmothoracids; Rs, residua; Ap, apusomonads. The position of apusomonads, Ap, was not considered when scoring the monophyly of “Rhizaria” as the position of this organism is highly variable, and it has been removed from recent classifications (see text). See Figure 4 for further notes. References cited in this figure are [,,–,,,–145].