Discussion of Phylogenetic Relationships
This tree is derived from a consensus of several different studies that are cited in the Discussion of Phylogenetic Relationships and the individual pages for each lineage shown.
Our understanding of eukaryotic relationships has been transformed by the use of molecular data to reconstruct phylogenies (Sogin et al., 1986). Prior to that, the diversity of microbial eukaryotes was vastly underestimated, and the relationships between them and multicellular eukaryotes were difficult to resolve (Taylor, 1978). Early molecular phylogenies based on small subunit ribosomal RNA (SSU rRNA) gene sequences suggested a ladder of basal lineages topped by a ‘crown’ composed of multicellular groups (animals, plants, and fungi) together with a subset of the purely microbial lineages (Sogin, 1989). A great number of the relationships revealed by SSU rRNA phylogeny have stood the test of time, but subsequent analyses based on protein coding genes and more recently very large datasets composed of hundreds of protein coding genes have led to a revision of the overall structure of the tree. The current view of eukaryotic phylogeny is of a small number of large ‘supergroups’, each comprising a spectacular diversity of structures, nutritional modes, and behaviours (Adl et al., 2005; Keeling, 2004; Keeling et al., 2005; Simpson and Roger, 2002). Some of these supergroup hypotheses are well supported, while others remain the subject of vigorous debate (see (Keeling et al., 2005) for a discussion of evidence). Furthermore the relationships between supergroups are poorly understood. Below we summarise the main members of each supergroup, the evidence for its monophyly, and emerging hypotheses for inter-supergroup relationships.
The Archaeplastida, or Plantae, comprises glaucophytes, red algae, green algae and plants. They are united by the possession of a plastid derived from primary endosymbiosis (see Symbiosis section). There has long been strong support for the monophyly of plastids in Archaeplastida based on molecular phylogeny and also plastid genome structure (Turner, 1997; Turner et al., 1999), and molecular phylogenies based on large numbers of protein coding genes have more recently demonstrated the monophyly of the nuclear/cytosolic lineage as well (Burki et al., 2008; Moreira et al., 2000; Reyes-Prieto et al., 2007).
Fig. 7. Some examples of Archaeplastida. From left to right, the red alga Chondracanthus (© Patrick Keeling), the green alga Cosmarium (© Patrick Keeling) and the land plants Typha latifolia (© Patrick Keeling) and Calocedrus decurrens (© 2008 Fort Photo).
Excavata is a large and diverse grouping that has been proposed based on a synthesis of morphological and molecular data. Many excavates share a similar feeding groove structure (from which the name is derived) (Simpson and Patterson, 2001; Simpson and Patterson, 1999). Many others lack this structure, but are demonstrably related to lineages that possess it in molecular phylogenies (Simpson, 2003; Simpson et al., 2006; Simpson et al., 2002). Putting this evidence together led to the suggestion of shared ancestry, and some recent multi-gene phylogenies in fact provide tentative support for the monophyly of the whole group (Burki et al., 2008; Rodriguez-Ezpeleta et al., 2007). Many excavates are anaerobes/microaerophiles and contain mitosomes or hydrogenosomes (e.g. diplomonads and parabasalids). Some are important parasites of animals (e.g. trypanosomes, Giardia). One lineage, the euglenids, includes photosynthetic species that have plastids derived from a green alga by secondary endosymbiosis (Breglia et al., 2007; Leander et al., 2007).
Fig. 8. Some examples of Excavata. From left to right: an SEM of the oxymonad Saccinobaculus minor (© Kevin Carpenter and Patrick Keeling), an SEM of the photosynthetic euglenid Lepocinclis spirogyra (© 2003 Brian S. Leander), a DIC light micrograph of the heterolobosean Stephanopogon minuta (© Naoji Yubuki and Brian S. Leander) and a fluorescence micrograph of the parabasalid Holomastigotes elongatum (© Guy Brugerolle).
Chromalveolates comprises six major groups of primarily single celled eukaryotes: apicomplexans, dinoflagellates and ciliates are members of the alveolates, they are hypothesised to be related to stramenopiles, cryptomonads, and haptophytes (Cavalier-Smith, 2004; Keeling, 2009). The basis for this hypothesis is the widespread presence of plastids in these groups that are all derived from secondary endosymbiosis with a red alga. It was therefore proposed that all chromalveolates share a common ancestor where this endosymbiosis took place (Cavalier-Smith, 1999). The monophyly of the plastids has been demonstrated with limited sampling (Hagopian et al., 2004; Rogers et al., 2007; Yoon et al., 2002), and some phylogenies inferred from many different nuclear genes show that the Chromalveolata are monophyletic with the Rhizaria nested within (see below) (Hackett et al., 2007). Additional support comes from two genes with unusual evolutionary histories involving lateral gene transfer and/or re-targeting to the plastid that are most consistent with a common origin of chromalveolate plastids (Fast et al., 2001; Harper and Keeling, 2003; Patron et al., 2004).
Fig. 9. Some examples of chromalveolates. From left to right: the multiculluar brown alga Macrocystis (© Tom Gruber), the diatom Stephanodiscus (© David G. Mann; this image is derived from the Professor Frank Round Image Archive at the Royal Botanic Garden Edinburgh), the ciliate Bursaria truncatella (© William Bourland, Freshwater and terrestrial microbes of Idaho), the filamentous dinoflagellate Gymnodinium catenatum (© Bob Andersen and D. J. Patterson; this image is of material from Provasoli-Guillard National Center for Culture of Marine Phytoplankton), and the bicosoecid Bicosoeca petiolata (© William Bourland, Freshwater and terrestrial microbes of Idaho).
Rhizaria comprises several very large and diverse groups of amoebae, flagellates and amoeboflagellates (Cavalier-Smith and Chao, 2003). Many of these will not be familiar to many readers, but they are ubiquitous in nature and important predators in many environments. Major lineages include Cercozoa, Foraminifera, and Radiolaria. Rhizaria is the most recently recognized supergroup, having been identified exclusively from molecular phylogenetic reconstruction (Cavalier-Smith, 2002; Cavalier-Smith, 2003; Nikolaev et al., 2004). Prior to this, there was little reason to anticipate this grouping, because there is no major structural character that unites them. (Although the amoeboid members of the group tend to produce fine pseudopodia, rather than the broad pseudopodia seen in many Amoebozoa – see below.) However, analyses of molecular phylogenies based on nearly all genes examined, as well as rare molecular markers such as insertions and deletions, initially identified the Cercozoa as a group that has then expanded to include the Foraminifera and eventually the Radiolaria (Archibald et al., 2002; Bass et al., 2005; Burki et al., 2007; Burki et al., 2008; Keeling, 2001; Longet et al., 2003; Moreira et al., 2007; Nikolaev et al., 2004; Polet et al., 2004). Analyses of multiple protein coding genes have further supported the monophyly of Rhizaria, and suggested a relationship to chromalveolates (see below).
Fig. 10. Some examples of Rhizaria. From left to right: the euglyphid amoeba Corythion dubium (© Edward Mitchell), the chlorarachniophyte Gymnochlora (© Patrick Keeling), the foraminiferans Allogromia (© Jan Pawlowski and José Fahrni) and Calcarina spengleri (© 2008 Michael).
Opisthokonta is a grouping consisting of Animals (Metazoa), the true Fungi and their close protistan relatives. The closest relatives of animals include choanoflagellates, which are free-living unicellular or colonial flagellates, and the parasitic Ichthyosporea (also known as Mesomycetozoea). Fungi are most closely related to a group of amoebae called nucleariids. Opisthokonts share two conspicuous features that are uncommon in other eukaryotes: Almost all cells in this group have flat mitochondrial cristae, while flagellated cells typically have a single emergent flagellum that inserts at the posterior end of the cell (Cavalier-Smith, 1987). The monophyly of this group has been shown convincingly by molecular phylogenies (Baldauf and Palmer, 1993; Lang et al., 1999; Ragan et al., 1996; Ruiz-Trillo et al., 2006; Steenkamp et al., 2006; Wainright et al., 1993), and also by a large, conserved insertion within the protein Elongation Factor 1-alpha (Baldauf and Palmer, 1993; Steenkamp et al., 2006). Recently a possible shared lateral gene transfer has been reported (Huang et al., 2005).
Fig. 11. Some examples of opisthokonts. From left to right: the choanoflagellate Salpingoeca (© William Bourland), the animals Saimiri sciureus (squirrel monkey, © Luc Viatour) and Cyanea capillata (lion's mane sea jelly, © Patrick Keeling), the fungus Morchella (© Patrick Keeling), and the microsporidian Fibrillanosema crangonycis (© Leon White).
The Amoebozoa are a diverse collection of protozoan eukaryotes, almost all of which are amoebae (i.e. cells that produce pseudopodia, but lack flagella) for some or all of their life cycle. Many produce lobose or fan-shaped pseudopodia (in contrast to the elongate, fine pseudopodia typical of Rhizaria), although short, fine sub-pseudopodia are also common. Amoebozoa includes lineages of ‘lobose amoebae’ (e.g the well known Amoeba and Chaos), the lobose testate amoebae (with the cell enclosed in a shell), most of the lineages of ‘slime molds’, the pelobionts and Entamoebae, which lack classical mitochondria, and a few mitochondriate flagellates. Amoebozoa were only recently united as group. Detailed microscopy studies had shown that amoebae as a whole were polyphyletic, and thus when early molecular phylogenetic studies based especially on ribosomal RNA sequences placed slime molds, lobose amoebae, pelobionts and entamoebae as multiple independent lineages (Hinkle et al., 1994; Sogin, 1989), this result seemed plausible. In the last few years, increasingly sophisticated molecular phylogenies incorporating many more taxa and/or genes have tended to unite these previously disparate groups (Bapteste et al., 2002; Fahrni et al., 2003), though not always with strong statistical support. A recent study suggests that the pseudopodia-producing flagellate Breviata represents the deepest branch within a monophyletic amoebozoa clade (Minge et al., 2008).
Fig. 12. Some examples of amoebozoans. From left to right: the slime mold Leocarpus fragilis (© 2008 Mavi Rodriguez Garcia), the slime mold Diachea leucopodia (© 2006 Randy Darrah, The Eumycetozoan Project, University of Arkansas), and a lobosean testate amoeba, likely Nebela tubulosa (© 2009 Antonio Guillén, identified by Ralf Meisterfeld).
'Unikonts': A Clade Consisting of Opisthokonts & Amoebozoans
There is now considerable evidence from molecular phylogenies that the opisthokonts and amoebozoans are closely related (Baldauf et al., 2000; Bapteste et al., 2002), and they also share a handful of other molecular characteristics in common (Richards and Cavalier-Smith, 2005). They have been proposed to be a clade called ‘unikonts’ because many of these organisms have a single flagellum (Cavalier-Smith, 2002), but biflagellated lineages are also known in this group. The root of the tree of eukaryotes has been proposed to be somewhere near this lineage, so it is possible the ‘unikonts’ are paraphyletic (Stechmann and Cavalier-Smith, 2002; Stechmann and Cavalier-Smith, 2003).
There has long been very strong evidence from several kinds of data for the monophyly of alveolates. Multi-gene trees have also consistently and strongly supported a relationship between alveolates and stramenopiles (Burki et al., 2007; Burki et al., 2008; Hackett et al., 2007; Patron et al., 2007; Rodriguez-Ezpeleta et al., 2005; Rodriguez-Ezpeleta et al., 2007; Simpson et al., 2006). There is now also very strong evidence from molecular phylogenies and a shared lateral gene transfer for the monophyly of cryptomonads, haptophytes, and their relatives (Burki et al., 2008; Hackett et al., 2007; Patron et al., 2007; Rice and Palmer, 2006). In addition there is evidence from the plastid genome and plastid targeted proteins for the monophyly of chromalveolates and their plastids (Fast et al., 2001; Hagopian et al., 2004; Harper and Keeling, 2003; Patron et al., 2004; Rogers et al., 2007; Yoon et al., 2002). However, multi-gene trees also consistently show that the entire rhizarian supergroup is closely related to alveolates and stramenopiles (Burki et al., 2007; Burki et al., 2008; Hackett et al., 2007; Rodriguez-Ezpeleta et al., 2007), and some support the monophyly of chromalveolates as a whole with the Rhizaria nested within the group. These relationships will doubtless be refined with further data, but for now we follow the consensus of the available evidence and place the Rhizaria within the Chromalveolata.
No one has provided updates yet.