Which Of The Following Is The Eukaryotic Supergroup That Contains Fungi And Animals?

• Journal List
• PLoS Genet
• v.2(12); 2006 Dec
• PMC1713255

PLoS Genet. 2006 Dec; 2(12): e220.

Evaluating Back up for the Current Classification of Eukaryotic Diverseness

Laura Wegener Parfrey

ⁱ Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, United States of America

Erika Barbero

² Department of Biological Sciences, Smith College, Northampton, Massachusetts, United states

Elyse Lasser

² Department of Biological Sciences, Smith College, Northampton, Massachusetts, The states of America

Micah Dunthorn

ⁱ Program in Organismic and Evolutionary Biology, University of Massachusetts, Amherst, Massachusetts, Us of America

Debashish Bhattacharya

^three Department of Biological Sciences, University of Iowa, Iowa City, Iowa, The states of America

^iv Roy J. Carver Centre for Comparative Genomics, University of Iowa, Iowa City, Iowa, The states

David J Patterson

⁵ Bay Paul Middle for Genomics, Marine Biological Laboratory, Woods Hole, Massachusetts, United States of America

Laura A Katz

¹ Program in Organismic and Evolutionary Biological science, Academy of Massachusetts, Amherst, Massachusetts, U.s.

ⁱⁱ Department of Biological Sciences, Smith Higher, Northampton, Massachusetts, U.s. of America

David Yard Hillis, Editor

Received 2006 May 11; Accustomed 2006 Nov ix.

Abstruse

Perspectives on the classification of eukaryotic diversity accept inverse quickly in recent years, equally the four eukaryotic groups inside the five-kingdom classification—plants, animals, fungi, and protists—take been transformed through numerous permutations into the current organisation 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. Nosotros evaluate the stability and support for the current half dozen-supergroup classification of eukaryotes based on molecular genealogies. We appraise 3 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 back up for monophyly when a supergroup is included as an out-group in phylogenetic studies targeting other taxa. Our assay demonstrates that supergroup taxonomies are unstable and that support for groups varies tremendously, indicating that the current classification scheme of eukaryotes is probable premature. We highlight several trends contributing to the instability and discuss the requirements for establishing robust clades within the eukaryotic tree of life.

Synopsis

Evolutionary perspectives, including the nomenclature of living organisms, provide the unifying scaffold on which biological knowledge is assembled. Researchers in many areas of biology use evolutionary classifications (taxonomy) in many ways, including equally a means for interpreting the origin of evolutionary innovations, equally a framework for comparative genetics/genomics, and as the basis for drawing wide conclusions nigh the diversity of living organisms. Thus, information technology is essential that taxonomy be robust. Hither the authors evaluate the stability of and support for the current classification system of eukaryotic cells (cells with nuclei) in which eukaryotes are divided into 6 kingdom level categories, or supergroups. These six supergroups unite diverse microbial and macrobial eukaryotic lineages, including the well-known groups of plants, animals, and fungi. The authors appraise the stability of supergroup classifications through time and reveal a rapidly changing taxonomic landscape that is difficult to navigate for the specialist and generalist alike. Additionally, the authors notice variable support for each of the supergroups in published analyses based on Dna sequence variation. The back up for supergroups differs co-ordinate to the taxonomic area under report and the origin of the genes (eastward.k., nuclear, plastid) used in the analysis. Encouragingly, combining a bourgeois approach to taxonomy with increased sampling of microbial eukaryotes and the use of multiple types of data is likely to produce a robust scaffold for the eukaryotic tree of life.

Introduction

Biological research is based on the shared history of living things. Taxonomy—the science of classifying organismal diversity—is the scaffold on which biological knowledge is assembled and integrated into a cohesive structure. A comprehensive eukaryotic taxonomy is a powerful inquiry tool in evolutionary genetics, medicine, and many other fields. As the foundation of much subsequent research, the framework must, yet, exist robust. Here nosotros test the existing framework by evaluating the support for and stability of the classification of eukaryotic diversity into six supergroups.

Eukaryotes (organisms containing nuclei) encompass incredible morphological diverseness from picoplankton of only two microns in size to the blue whale and giant sequoia that are eight orders of magnitude larger. Many evolutionary innovations are found only in eukaryotes, some of which are present in all lineages (e.chiliad., the cytoskeleton, nucleus) and others that are restricted to a few lineages (east.g., multicellularity, photosynthetic organelles [plastids]). These and other eukaryotic features evolved inside microbial eukaryotes (protists) that thrived for hundreds of millions of years before they gave rise independently to multicellular eukaryotes, the familiar plants, animals, and fungi [1]. Thus, elucidating the origins of novel eukaryotic traits requires a comprehensive phylogeny—an inference of organismal relationships—that includes the diverse microbial lineages.

Higher-level classifications have historically emphasized the visible diverseness of large eukaryotes, every bit reflected by the establishment of the constitute, fauna, and fungal kingdoms. In these schemes the diverse microbial eukaryotes take generally been placed in one (Protista [2–4] or Protoctista [five]) or two (Protozoa and Chromista [six]) groups (Figure one; merely come across also [7,8]). However, this historic distinction between macroscopic and microscopic eukaryotes does not fairly capture their circuitous evolutionary relationships or the vast diversity within the microbial world.

Trends in the Taxonomy of Eukaryotes

A comparison of 4 representative taxonomies illustrates trends within eukaryotic taxonomy over the past 50 years [2,5–7]. Movement of taxa is traced from before 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 grouping (right of line). Dashed lines indicate that a subset of members (left) is incorporated into subsequent groups (correct).

In the by decade, the emphasis in loftier-level taxonomy has shifted away from the historic kingdoms and toward a new system of six supergroups that aims to portray evolutionary relationships between microbial and macrobial lineages. The supergroup concept is gaining popularity every bit evidenced by several reviews [9,10] and inclusion in forthcoming editions of introductory biology textbooks. In addition, the International Gild of Protozoologists recently proposed a formal reclassification of eukaryotes into 6 supergroups, though acknowledging uncertainty in some groups [7].

The Supergroups

Below we introduce the 6 supergroups in alphabetical order (Effigy 2). The supergroup "Amoebozoa" was proposed in 1996 [11]. Original evidence for the group was drawn from molecular genealogies and morphological characters such as eruptive pseudopodia and branched tubular mitochondrial cristae. Notwithstanding, no articulate synapomorphy—shared derived character—exists for "Amoebozoa." In fact, amoeboid organisms are not restricted to the "Amoebozoa," but are found in at least iv of the six supergroups.

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).

The "Amoebozoa" include a multifariousness of predominantly amoeboid members such every bit Dictyostelium discoideum (cellular slime mold), which is a model for understanding multicellularity [12]. Some other member, Entamoeba histolytica, is an amitochondriate amoeba (Pelobiont) and is the cause of amoebic dysentery, an intestinal infection with global health consequences [13].

"Chromalveolata" was introduced equally a parsimonious, admitting controversial, explanation for the presence of plastids of ruddy algal origin in photosynthetic members of the "Alveolata" and "Chromista" [14]. Under this hypothesis, the last common antecedent of the chromalveolates was a heterotroph that acquired photosynthesis by engulfing a red alga and retaining it as a plastid [15,sixteen]. The "Alveolata" include ciliates, dinoflagellates, and apicomplexa, and its monophyly is well supported by morphology and molecules. "Chromista" was created as a kingdom to unite various microbial lineages with crimson algal plastids (and their nonphotosynthetic descendants) [6,17], but no articulate synapomorphy unites this clade.

The supergroup "Chromalveolata" includes microbes with disquisitional roles in the surround and in man health. Numerous primal discoveries emerged from studies of the model organism Tetrahymena (ciliate: "Alveolata"), including self-splicing RNAs and the presence of telomeres [xviii]. Phytophthora (stramenopile: "Chromista"), a soil-home organism, is the causative agent of the Irish gaelic Tater Famine [nineteen], whereas Plasmodium (Apicomplexa: "Alveolata") is the causative agent of malaria [20].

"Excavata" is a supergroup equanimous predominately of heterotrophic flagellates whose antecedent is postulated to have had a synapomorphy of a conserved ventral feeding groove [21]. Most members of "Excavata" are free-living heterotrophs, simply there are notable exceptions that are pathogens. For example, Giardia (Diplomonada) causes the intestinal infection giardiasis, and Trichomonas vaginalis (Parabasalia) is the causative agent of a sexually transmitted illness [22]. Kinetoplastids, such as Trypanosoma (Euglenozoa), take unique molecular features such as extensive RNA editing of mitochondrial genes that is templated by minicircle DNA [23].

"Opisthokonta" includes animals, fungi, and their microbial relatives. This supergroup emerged from molecular gene trees [24] and is united by the presence of a single posterior flagellum in many elective lineages [25]. Molecular studies have expanded microbial membership of the group and revealed a potential molecular synapomorphy, an insertion in the Elongation Gene 1α cistron in lineages containing this ortholog [26,27].

"Opisthokonts" include many biological model organisms (Drosophila, Saccharomyces). Vast amounts of research have been conducted on members of this supergroup and much textbook science is based on inferences from these lineages. Other notable opisthokonts include Encephalitozoon (Microsporidia: Fungi), a causative agent of diarrhea, which has one of the smallest known nuclear genomes at 2.nine MB [28]. Likewise included within the "Opisthokonta" are the choanoflagellates (e.one thousand., Monosiga), which are the sister to animals [29].

The supergroup "Plantae" was erected as a kingdom in 1981 [30] to unite the 3 lineages with chief plastids: light-green algae (including state plants), rhodophytes, and glaucophytes. Under this hypothesis a unmarried ancestral primary endosymbiosis of a cyanobacterium gave rise to the plastid in this supergroup [31]. The term "Plantae" has been used to describe numerous subsets of photosynthetic organisms, but in this manuscript will only be used in reference to the supergroup.

Well-known "Plantae" genera include Arabidopsis, a model angiosperm, and Porphyra (red alga), the edible seaweed nori. Within the "Plantae" there have been numerous independent origins of multicellularity including: Volvox (Chlorophyta) [32], the land plants, and red algae.

"Rhizaria" emerged from molecular data in 2002 to unite a heterogeneous group of flagellates and amoebae including: cercomonads, foraminifera, diverse testate amoebae, and former members of the polyphyletic radiolaria [33]. "Rhizaria" is an expansion of the "Cercozoa" [half dozen] that was too recognized from molecular data [34,35]. "Cercozoa" and foraminifera appear to share a unique insertion in ubiquitin [36], but there is a paucity of non-molecular characters uniting members of "Rhizaria."

"Rhizaria" encompasses a diversity of forms, including a heterotrophic flagellate Cercomonas (Cercomonada: "Cercozoa") and a photosynthetic amoeba Paulinella chromatophora, (Silicofilosea: "Cercozoa"). The latter likely represents a recent endosymbiosis of a cyanobacterium [37,38]. Some members of the "Rhizaria," notably the shelled foraminifera, besides have a substantial fossil tape that tin can exist used to determine the historic period of sediments [39].

Our Approach

To assess the robustness of the six proposed supergroups, we compare formal taxonomies and track group composition and nomenclature beyond time (Figures i and ​ 3). We also evaluate back up for the six supergroups by analyzing published molecular genealogies that either target a specific supergroup or aim to survey all supergroups. Our focus on molecular genealogies is limited. We recognize that supergroups have, in many cases, been divers by suites of characters such equally flagellar apparatus in "Excavata" [33,twoscore] and "Opisthokonta"[25], and that groups are more robust when supported by multiple data types (see Discussion). Use of genealogies is further complicated because a genealogy is the reconstruction of the history of a gene, and may or may not be coinciding with phylogenies, which depict the history of organisms [41,42]. Despite these factors, our treatment of molecular genealogies is warranted given the prevalence of molecular analyses in the literature that seeks back up for supergroups and the reliance on these gene trees in establishing taxonomy.

Trends in Supergroup Taxonomy

A comparison of 3 formal classifications illustrates trends inside (A) "Amoebozoa" [7,45,47]; (B) "Excavata" [7,33,lx]; (C) "Plantae" [2,half dozen,7]; and (D) "Rhizaria" [6,7,33]. A bulk of solid, horizontal lines would indicate temporal stability of supergroup classification. For visual simplicity nosotros do not betoken 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 farther notes.

For each genealogy we evaluate the taxon sampling for the targeted supergroup (Membership; Figures four–9) and the monophyly of all supergroups with at least two fellow member taxa (Supergroup monophyly; Figures 4–9). Monophyletic clades, those that include an ancestor and all of its descendants [43], are scored (+; Figures four–9). We assess support for supergroups when they are targeted past specific studies and when they are included every bit out-groups in studies targeting other supergroups. A conservative measure of out-grouping monophyly was used because we required merely 2 fellow member lineages be present. In dissimilarity, focal supergroups had broader taxonomic sampling.

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 diverseness [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 bachelor. Supergroup definition based on Adl et al. 2005 [four]: 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 (run into text). Some nodes were constrained in reference [97]. References cited in this figure are [25,33,45,48,49,84,97,114,115].

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 non considered when scoring the monophyly of "Rhizaria" as the position of this organism is highly variable, and it has been removed from contempo classifications (run across text). See Figure iv for further notes. References cited in this effigy are [33,49,57–59,61,131,140–145].

Results

Taxonomic Instability

There is considerable instability in taxonomies of the six putative supergroups (Figure 3). Causes of the rapid revisions in eukaryotic taxonomy over short time periods include: (1) nomenclatural ambiguity, (2) imperceptible and poorly supported higher-level taxa, and (three) nomenclature schemes erected under differing taxonomic philosophies. For example, taxonomy of the "Amoebozoa," a term originally introduced by Lühe in 1913 [44] to comprehend a very different aggregation of organisms, has changed considerably in ten years (Figure 3A). "Variosea" was created as a subclade within the "Amoebozoa" in 2004 to group taxonomically unplaced genera of amoebae with "exceptionally varied phenotype" [45]. Rarely supported past morphology or molecular evidence [46–49], this taxon was excluded from subsequent classifications [vii,47] just is still discussed in the literature [46]. Similarly, the excavate taxon "Loukozoa" [six] has been continually redefined to include a multifariousness of taxa bearing a ventral groove (Figure iiiB) and finally abased [40]. The taxonomy of "Rhizaria" has emerged largely from molecular genealogies and has varied partly in response to shifting topology of gene trees that modify with taxon sampling and the method of tree construction [6,33,50,51] (Figure 3D).

The taxonomy of "Plantae" is destabilized by the complex history of the term. Used since Haeckel's time [52], "Plantae" has been redefined numerous times to describe various collections of photosynthetic organisms, leading to major discrepancies between taxonomic schemes (Figure iiiC; e.g., [2,five]). The term "Archaeplastida" was recently introduced to alleviate confusion over "Plantae," just this synonym is not widely used.

The stability of two supergroups, "Chromalveolata" and "Opisthokonta," cannot be assessed at this time considering only a single formal taxonomy exists [7]. Other nomenclature schemes of eukaryotes segregate animals and fungi every bit separate kingdoms and identify microbial opisthokonts in the kingdom Protozoa (Figure 1) [6,33]. Similarly, chromalveolate members are ofttimes divided between the polyphyletic kingdoms "Chromista" and "Protozoa" (Figure 1) [33,49].

Varying Support for Membership within and Monophyly of Targeted Supergroups

Several supergroups are mostly well supported when targeted in molecular systematic studies. Strikingly, the monophyly of both the original and expanded "Opisthokonta" members is strongly supported in all investigations targeting the group (ten of x, Figure 7). 2 other supergroups are also well supported: "Rhizaria" monophyly is recovered in 11 of 14 studies focusing on this supergroup (Figure nine) and "Amoebozoa" retained in 5 of seven topologies (Figure 4). However, support for these groups is expected, given that they were recognized from molecular gene trees [eleven,33].

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" every bit this organism is highly variable, and information technology has been removed from recent classifications (encounter text). Run into Figure 4 for further notes. References cited in this figure are [24–27,33,49,115,122,129–132].

"Excavata" rarely form a monophyletic group in molecular systematic studies targeting this supergroup (ii of nine; Figure 6). Moreover, the position of putative members, jakobids, Malawimonas, parabasalids, and Diphylleia vary by analysis (Effigy 6). Three distinct subclades, all of which are supported by ultrastructural characters [40], are more often than not recovered (Fornicata [half dozen of half-dozen], Preaxostyla [six of six], and Discicristata [five of eight]; Figure 6).

Back up 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 + European union) 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 four for further notes. References cited in this figure are [33,xl,49,threescore,115,123–128].

Support for two supergroups varies depending on the blazon of graphic symbol used: plastid or nuclear. The monophyly of "Plantae" and "Chromalveolata" are well supported by plastid characters: four of iv plastid analyses (Figure 8) and six of nine (Figure 5), respectively. The "Plantae" clade is monophyletic in merely three of six analyses using nuclear genes, including Elongation Factor 2 [53] and a 100+ cistron assay that included very limited taxon sample [54]. Nuclear loci never support "Chromalveolata" (zero of six; Figure 5), though alveolates and stramenopiles often form a clade to the exclusion of haptophytes and cryptophytes (e.g., [24,97]; Figures 4 and seven​ ).

Support for Membership and Supergroup Monophyly from "Chromalveolata"-Targeted Molecular Genealogies

Fellow member taxa: Al, Alveolata; St, Stramenopiles (Heterokonts); Ha, Haptophyta; Cr, Cryptophyceae. Monophyletic "Plantae" from plastid genealogies includes secondarily derived plastids. Encounter Effigy 4 for further notes. References cited in this figure are [33,49,55,56,107,108,115–122].

Loc, location (genome) from which the cistron of interest originated; Pla, plastid genome; Nuc, nuclear genome; Mit, mitochondrial genome.

Support for Membership and Supergroup Monophyly from "Plantae"-Targeted Molecular Genealogies

Member taxa: Gr, Chloroplastida = Viridiplantae (Greenish algae, including land plants); Rd, Rhodophyceae (Red algae); Gl, Glaucophyta. See Effigy 4 for full general notes and Figure 5 for plastid-specific notes. References cited in this figure are [33,49,53,54,115,133–139].

Decreased Support for Monophyly of Supergroups as Out-Groups in Other Studies

For each genealogy we likewise assessed the monophyly of the supergroups when included as out-groups. Overall, we find that support for the monophyly of a given supergroup is stronger when targeted and back up decreases when the same supergroup is included as an out-grouping in other studies.

This trend is particularly unexpected given our less stringent requirements for monophyly of out-groups: a minimum of only ii members need be included, while targeted groups had broader taxon sampling (see Methods). A priori, it would seem that the lower stringency could allow a limited sample of supergroup members to substitute for overall supergroup monophyly, thereby increasing the occurrence of supergroup monophyly for out-group taxa. However, this scenario is realized only in the groups that receive poor back up, "Excavata" and "Chromalveolata," assessed by nuclear genes. "Excavata" is monophyletic more frequently when members are included as out-groups (7 of xxx, Figures iv, ​ 5, and seven–nine, versus ii of nine, Figure 8). Taxonomic sampling of these lineages is often considerably lower in non-targeted assay, and monophyly reflects that of the subclades "Discicristata" or "Fornicata" (such as in [48,58,59], but see [sixty,128] for ii exceptions, Figures 4, ​ six, and ​ ix). "Chromalveolata" is monophyletic in ten of 45 nuclear gene trees targeting other taxonomic areas (Figures four and ​ 6–9). Intriguingly, in all ten of the cases where nuclear genes support monophyletic "Chromalveolata," only alveolates and stramenopiles are included (Figures 4–9).

In dissimilarity, the remaining supergroups are monophyletic less often when included every bit out-groups. For example, "Opisthokonta" was recovered in all studies targeting this supergroup, but in just 33 of 41 studies that target other groups (Figures 5–nine). Similarly, both the "Amoebozoa" and "Rhizaria" are monophyletic less often when their members are included as out-groups in studies targeting the remaining five supergroups (15 of 35 and eight of 15, respectively: Figures 5–9 and ​ 4–8). When included as an out-group, "Plantae" plastids usually class a monophyletic clade (8 of ix analyses, Effigy 5) merely back up is much lower in nuclear factor trees (11 of 42, Figures 4–vii and ​ 9).

Discussion

Our assay reveals varying levels of stability and support for the 6 supergroups (Effigy 2). Below, we appraise the status of each supergroup, describe factors that contribute to the instability, and propose measures to improve reconstruction of an accurate eukaryotic phylogeny.

Supergroup Robustness

Robust taxa—those consistently supported by multiple datasets—are emerging and include the supergroup "Opisthokonta." This group of animals, fungi, and their microbial relatives receives consistent support in molecular genealogies. This supergroup was monophyletic in 43 of 51 trees we examined (Figures 4–ix). "Opisthokonta" is also united by additional types of data: most members share a single posterior flagellum, contain plate-like cristae in mitochondria, and have an insertion within the Elongation Factor 1α gene [8,25–27].

The remaining v supergroups receive varying degrees of back up from molecular genealogies. "Amoebozoa" and "Rhizaria" received loftier support in analyses that targeted them (Figures four and ​ 9, respectively) simply formed monophyletic clades less oft when included as out-groups. The ii photosynthetic clades "Chromalveolata" and "Plantae" receive differential back up depending on the origin of the gene: high support in plastid genealogies merely low in nuclear cistron trees (Figures 5 and ​ eight, see Results). Molecular support for the "Excavata" as a whole is defective from well-sampled gene trees (Figure 6).

Although the six supergroups are non consistently supported past molecular genealogies, some nested clades are emerging as robust groups. For example, a sister relationship between Alveolata and Stramenopila is oftentimes recovered. It is this human relationship that makes "Chromalveolata" appear monophyletic in nuclear genealogies when only these clades are included as outgroups (due east.k., [24,97], and Figures ​ 4 and ​ 7). In that location is also growing support for several subgroups within the poorly supported "Excavata" (i.east., "Fornicata" and "Preaxostyla"; Figure vi).

Alternative Hypotheses

Although it is clear from our analysis that eukaryotic supergroups are not well supported, no culling loftier-level groupings emerge from molecular genealogies. Rather, there is back up for lower-level groups, such every bit the "Excavata" subgroups discussed above and maybe besides alveolates plus stramenopiles. This suggests that either there are no higher-level groupings to exist found, or in that location is equally yet inadequate data to resolve these clades. We believe that lack of taxon sampling is the key to resolution.

Farther evidence against the vi-supergroup view of eukaryotic multifariousness is the being of "nomadic" taxa—lineages that exercise non have a consistent sister grouping, but instead wander between various weakly supported positions. Some nomadic taxa are acknowledged incertae sedis (of unknown taxonomic position) such equally Ancyromonas, Breviata, and Apusomonadidae [7,8]. Other taxa that have been assigned to supergroups likewise announced to be nomadic, including Haptophyta (putative member of "Chromalveolata") and Malawimonas (putative member of "Excavata"). For example, the haptophytes variously branch with Centrohelida and red algae [45], sister to a clade of "Rhizaria" and Heterolobosea [48], sister to cryptophytes [56], and in a basal polytomy [61]. These nomadic taxa may either represent independent, early diverging lineages or their phylogenetic position cannot yet exist resolved with the information available. Again, nosotros feel that taxon sampling is the central in society to distinguish between these possibilities.

Why Is Eukaryotic Taxonomy So Difficult?

The variable support for relationships is in part attributable to the inherent difficulty of deep phylogeny, the chimeric nature of eukaryotes, misidentified organisms, and conflicting approaches to taxonomy. Here nosotros elaborate on these destabilizing trends and provide illustrative examples.

Challenges of deep phylogeny.

Reconstructing the history of eukaryotic lineages requires extraction of phylogenetic signal from the dissonance that has accumulated over many hundreds of millions of years of divergent evolutionary histories. There is doubt whether resolution of divergences this deep can exist resolved with molecular data [62]. Additionally, the nature of the relationships may besides pose a significant challenge. For case, a rapid radiation of major eukaryotic lineages has been proposed [63] and is the most difficult scenario to resolve because of the lack of time to accrue synapomorphies at deep nodes.

Farther, phylogenetic relationships tin exist obscured by heterogeneous rates of evolution and divergent selection pressures. For case, genes in many parasitic lineages of eukaryotes experience elevated rates of evolution. If not properly deemed for, these fast lineages volition grouping together due to long-branch attraction [64,65]. This was the case for Microsporidia, intracellular parasites of animals; early small subunit rDNA (SSU) genealogies placed the Microsporidia at the base of the tree with other amitochondriate taxa, including Giardia and Entamoeba [66]. These parasites were united under the "Archezoa" hypothesis [67]. More recent analyses with appropriate models of evolution [68] and those using protein-coding genes [69] place the Microsporidia inside fungi and falsify "Archezoa." This example demonstrates the importance of phylogenetic methods in the interpretation of eukaryotic diversity. In our analysis we observe no clear correlation between method of tree building and group stability. Arguments near phylogenetic inference take been discussed extensively [62,seventy–76], and increasingly sophisticated algorithms are being developed to compensate for the difficulties [77–79].

The chimeric nature of eukaryotes.

Reconstructing the history of eukaryotic lineages is complicated by the horizontal transfer of genes and organelles [74,fourscore–83]. For instance, "Chromalveolata" plastid genes tell i story, consistent with a unmarried transfer from crimson algae, which is non currently supported by bachelor nuclear genes (Figure v). In that location is likewise a growing body of evidence for aberrant lateral cistron transfers in eukaryotes (reviewed in [80,82]).

Instability due to misidentification.

Misidentification destabilizes taxonomy because all efforts to allocate a misidentified organism reach erroneous conclusions. Cases of misidentification atomic number 82 to inaccurate conclusions and require considerable effort to remedy. At that place is a rigorous standard for identifying microbial eukaryotes, but this standard is not always upheld. For case, the putative "Amoebozoa" species "Mastigamoeba invertens" that always branched exterior the "Amoebozoa" clade [45,49,84] was misidentified [85]; it has now been properly described as Breviata anathema and is not yet placed within whatever of the supergroups [85].

Inaccurate conclusions about organismal relationships can likewise effect from contamination (e.g., from symbionts and parasites). The results of subsequent molecular genealogies are therefore wrong and misleading. For instance, opalinids, multinucleated flagellates that inhabit the lower digestive track of Anurans, were placed in the stramenopiles (Slopalinida: "Chromalevolata") based on ultrastructural data [86]. However, the first molecular sequences for this group placed them within fungi (Opalina ranarum and Cepedea virguloidea [87,88]). These sequences were later on shown to vest to zygomycete fungal contaminants, not to the opalinids. Subsequent isolates (Protoopalina intestinalis) yielded genealogies congruent with the ultrastructural data, placing P. intestinalis within the stramenopiles [89]. To avoid setbacks and confusion due to misidentification, nosotros suggest that all analyses of eukaryotic diversity include a vouchering organization for strains, images, and DNAs.

Conflicting approaches to taxonomy.

Our evaluation of the stability of taxonomy for supergroups reveals a apace changing landscape (Figures 1 and ​ iii). The instability in higher-level classifications of eukaryotes reflects the multifariousness of philosophical approaches, the exploratory land of eukaryotic taxonomy, and premature taxon naming. Many researchers seek schemes based on monophyletic groupings then that their taxonomies reflect evolutionary relationships [7,8,90,91]. In contrast, others employ a taxonomic philosophy in which evolutionary relatedness and monophyly are but 1 criterion from a set of grouping characteristics [33]. Paraphyly—a taxon divers without all descendants—is tolerated in these systems, and paraphyletic taxa are designated as such (see [6] p. 210–215 for caption of such a philosophy).

In many cases, nomenclature schemes that are separated by two years or less vary essentially from one another (e.g., Figure 3A and ​ threeB). New groups and fluctuating group limerick event in numerous cases of homonymy (two concepts linked to one name), synonymy (ane concept linked to two names), and redefinition of existing terms. For instance, at the highest level the terms "Amoebozoa," "Opisthokonta," and "Plantae" were all introduced under different definitions [4,44,52] before existence applied to supergroups. The term "Plantae" is an extreme case of homonymy having referred to numerous groups of photosynthetic organisms over the past century and a half (Effigy 3C). The rapidly changing taxonomic landscape makes it hard for not-specialists as well specialists to follow the current fence over supergroups.

Toward a Robust Scaffold to the Eukaryotic Tree of Life

Taxonomic sampling.

Possibly the most critical aspect of the electric current land of eukaryotic systematics is the very limited taxonomic sampling to date. This is particularly problematic as the supergroup literature is often derived from a resampled pool of genes and taxa. More than 60 lineages of microbial eukaryotes accept been identified past ultrastructure [eight], all the same only most one-one-half of these take been included in molecular analyses. Furthermore, even when these lineages are included, they are by and large represented past a unmarried species. Such sparse sampling increases the risk of long-branch attraction as discussed above, such as occurred for Giardia, and may cause artifactual relationships [92]. Farther, analyses of sequences from newly sampled lineages have altered or expanded supergroup definitions (east.g., nucleariids in "Opisthokonta" [93] and Phaeodarea in "Rhizaria" [94]). Thus, statements of monophyly may be premature when taxonomic sampling is low.

There is tension betwixt increasing the number of taxa versus the numbers of genes. Several theoretical works have demonstrated the diminishing returns of increased number of genes relative to increased taxon sampling [95–97], but see [98]. In addition, increasing taxon sampling can lead to shifts in molecular tree topology [99–101]. These results provide incentive to concentrate sequencing efforts on obtaining more taxa and a moderate number of genes. We recommend increasing the lineages sampled and the number of diverse taxa inside lineages. We are optimistic that equally information become available from a greater diversity of taxa, eukaryotic phylogeny volition become increasingly more resolved.

Multiple character sets.

We further anticipate that support for clades will increment equally additional character sets are incorporated. Phylogenies based on single characters, whether genes, morphology, or ultrastructure, are subject to biases in the data and are not reliable by themselves. Hence, multiple character sets should be used to approve results. Ultrastructural apomorphies combined with molecular genealogies have proven to be proficient indicators of phylogeny at the level below supergroups [xl,102]. This approach has bolstered support for "Fornicata" and "Preaxostyla," which are consistently recovered in molecular genealogies and have defining ultrastructural characters. As we movement forward with multiple character sets, nosotros must shift from searching for characters to support hypotheses to evaluating hypotheses in lite of all available data.

Well-sampled multigene and genome scale molecular systematics provide some other powerful tool for resolving aboriginal splits in the tree of life. The National Science Foundation initiative "Assembling the Tree of Life" provides evidence of this shift in systematics inquiry, whereby all proposals involve multigene or genome (organellar) sequencing to institute robust phylogenetic hypotheses (encounter http://world wide web.nsf.gov/pubs/2005/nsf05523/nsf05523.htm; [54,97]). The EuTree consortium (http://world wide web.eutree.org) aims to increase substantially the sampled diversity of eukaryotes by focusing on understudied lineages in our multigene project to assemble the tree of life.

An case of multigene study is analysis of genes involved in clade-specific functions. This approach has been employed in testing "Plantae" and "Chromalveolata" (due east.g., [103]). A single endosymbiosis (of a cyanobacterium in "Plantae" and red alga in "Chromalveolata") predicts that the systems that facilitate controlled commutation of metabolic intermediates between the symbiotic partners be shared past putative members of these ii supergroups [104]. This prediction has been supported by analyses of the plastid import machinery [105] and antiporters that transport fixed carbons across the plastid membranes [106]. However, taxon sampling has been express in these studies. Currently, increased sampling of genomes from diverse photosynthetic eukaryotes is yielding additional genes for clade-specific predictions [107,108].

A conservative approach to taxonomy.

Because taxonomy is the foundation for much of the dialog and inquiry in evolutionary biology, in that location must be an unambiguous taxonomic system in which one term is linked to ane concept. In contrast to this ideal, homonymy and redefinition are prevalent in the taxonomy of eukaryotes, often as the result of premature introduction or redefinition of taxa (run into in a higher place; Effigy 3). Emerging hypotheses benefit the community past sparking new research to test the hypothesis, but they also introduce ambiguity. To alleviate the defoliation, nosotros suggest introducing hypotheses equally informal groups and using inverted commas to betoken the beingness of a caveat, as done with the uncertain groups in this manuscript. These steps will inform the community that group limerick is probable to change, alleviate quick taxon turnover, and promote stable taxa that are more resistant to compositional modify.

As increasing amounts of data become available, well-supported nodes emerge and classifications tend to stabilize, such equally is occurring for the ordinal framework for angiosperms [109,110]. Similarly, we look that this bourgeois approach, combined with increased sampling of taxa and genes, volition promote the future stabilization of eukaryotic classification.

Conclusion

Although the level of back up varies amid groups, the current classification of eukaryotes into six supergroups is existence adopted broadly by the biological community (i.east., evidenced past its appearance in biology textbooks). The supergroup "Opisthokonta" and a number of nested clades within supergroups are supported past most studies. Withal, support for "Amoebozoa," "Chromalveolata," "Excavata," "Plantae," and "Rhizaria" is less consequent. The supergroups, and eukaryotic taxonomy in general, are farther destabilized by considerable fluidity of taxa, taxon membership, and ambiguous nomenclature as revealed past comparison of nomenclature schemes.

The accurate reconstruction of the eukaryotic tree of life requires: (1) a more than inclusive sample of microbial eukaryotes; (ii) distinguishing emerging hypotheses from taxa corroborated past multiple datasets; and (iii) a bourgeois, mutually agreed upon approach to establishing taxonomies. Analyses of these types of data from a broad, inclusive sampling of eukaryotes are likely to lead to a robust scaffold for the eukaryotic tree of life.

Methods

Stability of taxonomy.

To assess the stability of supergroup taxonomies over time, we selected three classification schemes for each supergroup and tracked both the stability of taxa membership (solid and dashed lines; Figures i and ​ 3) and the fate of newly created taxon names (asterisk; Figure 3). In sampling representative taxonomies, nosotros aimed to capture a variety of authors and opinions. In the case of "Opisthokonta" and "Chromalveolata" nosotros are aware of just one formal, peer-reviewed classification scheme [vii]. Given the lack of equivalency in ranks betwixt taxonomies, we have chosen to display three levels with the intention of listing equivalent levels clearly.

Membership support.

Within each supergroup, we assess the back up for each member taxon past documenting its inclusion in molecular genealogies (Figures 4–ix). Member taxa were called considering they are historically a well-supported group, normally with an ultrastructural identity. The haptophytes are such a group, and share a haptonema [viii]. Nosotros included members that represent a broad interpretation of the supergroup. For example, "Rhizaria" member taxa include groups (e.1000., apusomonads) originally placed in "Rhizaria" simply later removed. Nosotros considered a taxon to be a supported member of its supergroup (filled circles; Figures four–9) when it falls within a monophyletic clade containing a majority of the supergroup members. A taxon that falls outside of its supergroup clade, or on the occasion that a bulk of members do not grade a monophyletic clade, is considered unsupported in that genealogy (open up circles; Figures 4–9).

The inclusion of a genealogy requires that information technology be found in a newspaper that specifically addresses one of the supergroups or analyzes broad eukaryotic diverseness. The genealogies must likewise include adequate sampling—two-fellow member taxa per supergroup—from at to the lowest degree two of the six supergroups to allow for the comparing of supergroup monophyly. In cases where multiple gene copse are presented nosotros display the authors' findings as multiple entries when the copse are not congruent or as a unmarried entry when the trees are concordant. Due to the lack of monophyly in about all analyses, we have evaluated the support for several hypothesized subgroups within the "Excavata" (geometric shapes; Figure 6).

Supergroup monophyly.

To assess monophyly of supergroups, we used the set of genealogies described above to evaluate the molecular support for the supergroups as interpreted by Adl et al. 2005 ([7]; Figures 4–9). We analyzed the monophyly [43] of each supergroup in trees having at least two member taxa present (+/− Figures 4–ix). We practice not indicate the method of tree construction. Although the algorithm used is important, we did not observe a clear correlation betwixt supported groups and algorithm used. Nosotros were too liberal in accepting whatsoever level of support (e.g., bootstrap values and posterior probabilities ranged from 4%–100%) when determining monophyly, in office because there is fence over acceptable cutoff values [111–113].

Supporting Information

Accretion Numbers

Information about commonly used genes for phylogenesis of microbial eukaryotes discussed in this paper tin be plant in the Homologene database at NCBI (http://www.ncbi.nlm.nih.gov/Genbank): actin (88645), α-tubulin (81745), β-tubulin (69099), Elongation Gene 1α gene (68181), small subunit rDNA (6629), and ubiquitin (39626). Accession numbers for genes from misidentified organisms can exist found at NCBI in GenBank (http://www.ncbi.nlm.nih.gov/Genbank). Misidentified opalinids: Opalina ranarum ({"type":"entrez-nucleotide","attrs":{"text":"AF141969","term_id":"4929159","term_text":"AF141969"}}AF141969) and Cepedea virguloidea ({"blazon":"entrez-nucleotide","attrs":{"text":"AF141970","term_id":"4929160","term_text":"AF141970"}}AF141970); correctly identified Protoopalina intestinalis ({"blazon":"entrez-nucleotide-range","attrs":{"text":"AY576544-AY576546","start_term":"AY576544","end_term":"AY576546","start_term_id":"50898176","end_term_id":"50898178"}}AY576544-AY576546) and Breviata anathema ({"type":"entrez-nucleotide","attrs":{"text":"AF153206","term_id":"5524611","term_text":"AF153206"}}AF153206). Sequences for Encephalitozoon cuniculi tin can be institute at NCBI under genome project number 9545.

Acknowledgments

Many thanks to Giselle Walker for discussions about supergroups and for graciously sharing a manuscript of her own. The authors also give thanks John Logsdon and Toby Kiers for comments and Jan Pawlowski for helpful discussions on nomadic lineages.

Footnotes

Competing interests. The authors have declared that no competing interests exist.

A previous version of this article appeared as an Early Online Release on November 13, 2006 (doi:x.1371/journal.pgen.0020220.eor).

Writer contributions. LWP, EB, DJP, and LAK conceived and designed the experiments. LWP, EB, EL, and LAK analyzed the data. LWP, EB, MD, DB, DJP, and LAK wrote the paper.

Funding. This work is supported by the National Scientific discipline Foundation Assembling the Tree of Life grant (043115) to DB, DJP, and LAK.

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Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1713255/

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