1.2 The tree of eukaryotes
1.2.4 Groundwork for reconstructing
These profound modifications of the structure of the eukaryotic tree led to the concept that most, if not all, diversity can be assigned to one of several major assemblages: the
“supergroups” (Figure 5-ch.1). Reassembling the evolutionary history of eukaryotes was obviously not the result of a single study, but very much a matter of uniting several types of data into one comprehensive picture. Despite what has been mentioned above, single-gene trees continue to be a valuable source of information when they are combined with an appropriate knowledge of potential artifacts, because they are generally built with taxon-rich alignments. Thus, by correctly interpreting several individual trees one might be able to discern general tendencies in phylogenies. However, as more and more genomic data accumulated, it became possible to assemble larger datasets that contain in principle more phylogenetic signal, so great possibilities were given to address further evolutionary questions. Finally, discrete molecular characters such as indels, gene fusions, or gene order have also been useful in reevaluating the eukaryotic tree as they are independent of phylo-genetic reconstruction, although much caution is here as well required because these mark-ers are not free of misleading errors [Bapteste and Philippe 2002].
When this working hypothesis was first summarized in a paper, eight supergroups were recognized [Baldauf 2003]. This review was notably relevant because it accounted for the
“true diversity of life”, i.e. the discovery of non-cultured minute organisms, nano- or pico- in size, that were scattered across the tree. Soon after and regularly since then, reviews are being published updating the tree of eukaryotes with the lastest minor modifications, es-sentially representing the same scheme for the eukaryote evolution [Simpson and Roger 2004; Adl et al. 2005; Keeling et al. 2005; Lane and Archibald 2008]. These trees, unrooted,
all display a basal polytomy with five or six branches representing the supergroups that emerge from a common point, the order of divergence among these groups being very much uncertain (Figure 5-ch.1). Importantly, the supergroups hypothesis represents a con-sensus for the tree of eukaryotes, the most accurate we have so far, but by no means an unshakable scheme. The existence (that is, the monophyletic origin) for most of the super-groups is still highly arguable. Generally, parts of these hypothesized major assemblages have been reasonably shown to have a common origin, but we currently lack evidence for the supergroups as a whole, including all postulated lineages (this is less true for the opisthokonts, commonly robustly supported, see [Parfrey et al. 2006] for a broad discus-sion).
Figure 5-ch.1. One of the numerous schemes for the current view of the eukaryotic evolution, repre-senting the six hypothesized supergroups of eukaryotes. From [Lane and Archibald 2008].
Below I briefly introduce these six supergroups:
O p i s t h o k o n t s: This supergroup contains animals and fungi [Cavalier-Smith and Chao 1995], which are thought to have evolved independently from unicellular lineages belonging to the paraphyletic assemblage Choanozoa [Lang et al. 2002; Cavalier-Smith and Chao 2003c; Steenkamp et al. 2006; Ruiz-Trillo et al. 2008; Shalchian-Tabrizi et al.
2008], also included in it. It is putatively united by the presence of a single posterior flagellum in several representatives [Cavalier-Smith and Chao 1995], as well as much molecular-based evidence (e.g., single-genes [Baldauf and Palmer 1993; Wainright et al.
1993], 4 genes [Baldauf et al. 2000], 143 genes [Rodriguez-Ezpeleta et al. 2005], amino acid insertion/deletion [Baldauf and Palmer 1993]). It is currently the most reliable su-pergroup, but some continue to argue for a close evolutionary relationship between animals and green plants instead [Stiller 2007].
A m o e b o z o a: This supergroup includes mostly amoeboid protists (that is cells with pseudopodia) such as the classical amoeba with lobose pseudopodia but also slime moulds and some amitochondrial lineages. Evidence that it is a monophyletic group, not very strong at the moment, has emerged only recently and is based on single and multigene phylogenies [Baldauf et al. 2000; Bapteste et al. 2002; Fahrni et al. 2003;
Smirnov et al. 2005], as well as a gene fusion in mitochondrial genome of the two spe-cies that were investigated [Lonergan and Gray 1996].
Opisthokonts and Amoebozoa are often united in a larger supergroup, U n i k o n t s [Cavalier-Smith 2002], that is supported by several rare genomic changes (see section 1.2.5) [Stechmann and Cavalier-Smith 2002; Stechmann and Cavalier-Smith 2003b; Richards and Cavalier-Smith 2005] as well as several single (e.g., [Baldauf and Palmer 1993]) and a grow-ing number of multigene phylogenies (e.g., [Rodriguez-Ezpeleta et al. 2007a]).
P l a n t a e (or A r c h e p l a s t i d a ): This supergroup is comprised of the three main lineages of primary photosynthetic organisms, thus corresponding to the group where plastids with two membranes first evolved by primary endosymbiosis with a cyanobac-teria are found: glaucophytes, green plants, and red algae. Its monophyly has been gen-erally accepted because of the parsimonious explanation for a single origin of primary plastid [Palmer 2003; Keeling 2004; Mcfadden and van Dooren 2004; Reyes-Prieto et al.
2007; Archibald 2009] (although see [Prechtl et al. 2004; Nowack et al. 2008] for exam-ples of more recent independent primary endosymbioses), but other views, in particular an earlier divergence of the red algae, are still strongly debated [Nozaki et al. 2003; No-zaki 2005; NoNo-zaki et al. 2007; Stiller 2007; Maruyama et al. 2008]. The use of genomic data has recently recovered strong support for a monophyletic assemblage in several
studies, both based on chloroplast [Martin et al. 2002; Chu et al. 2004; Hagopian et al.
2004; Rodriguez-Ezpeleta et al. 2005] and nuclear genes [Rodriguez-Ezpeleta et al. 2005;
Rodriguez-Ezpeleta et al. 2007a].
C h r o m a l v e o l a t a: This supergroup is doubtlessly the most debated, because of the lack of clear and simple evidence supporting it and its central role in the under-standing of eukaryote evolution. It encompasses at present four diverse groups, mixing phototrophy and heterotrophy: stramenopiles (heterokonts), cryptomonads, haptophytes (altogether the chromists [Cavalier-Smith 1998a]), and alveolates. This grouping results from the proposition that the number of plastids originated by secondary endosymbiosis (i.e. involving two eukaryotes) should be limited in evolution because of the real com-plexity in establishing a protein targeting system in a nascent plastid [Cavalier-Smith 1999]. Specifically, the chromalveolate hypothesis postulates that a single secondary en-dosymbiosis with a red alga took place in the ancestor of all chromalveolates, giving rise to an orthologous plastid in all its descendants. The consequence of this is that the host lineages must be related, a condition that is generally not respected as a whole even with big alignments (haptophytes and cryptomonads often branch elsewhere in the tree, or are not supported as sister to the rest of the chromalveolates) [Harper et al.
2005; Patron et al. 2007], but see [Hackett et al. 2007]. On the other hand, plastid data often recover a common origin for the photosynthetic members of this supergroup [Yoon et al. 2002; Khan et al. 2007], but this does not rule out the possibility that the red plastids were acquired independently via serial endosymbioses to reach the current situation. In favor of the hypothesis are also two specific gene duplications that unde-niably cluster the plastid-targeted proteins of the chromalveolates [Harper and Keeling 2003; Patron et al. 2004], but the relationships of the cytosolic version are much more ambiguous.
R h i z a r i a: This supergroup is the most recently recognized assemblage and is pres-ently only defined based on molecular data, commonly including organisms bearing
“root-like reticulose or filose pseudopodia” [Cavalier-Smith 2002; Cavalier-Smith 2003].
In addition to typically amoeboid taxa, Rhizaria also include a large diversity of free-living flagellates, amoeboflagellates, and parasitic protists. The first presage for this grouping was a clade formed by the euglyphid testate amoebae and the photosynthetic chlorarachniophytes in SSU rRNA phylogeny [Bhattacharya et al. 1995]. This clade was later enlarged to also include zooflagellate species and the plasmodiophorid plant parasites [Cavalier-Smith and Chao 1996-1997], leading to the creation of the phylum
pected result was later confirmed by the discovery of a one or two amino acids inser-tion in the polyubiquitin polymers [Archibald et al. 2003a; Bass et al. 2005], and analy-ses of the large subunit of RNA polymerase gene [Longet et al. 2003] and SSU rDNA [Berney and Pawlowski 2003]. The taxonomic composition of Cercozoa was progres-sively expanded by including various zooflagellates [Atkins et al. 2000; Kuhn et al.
2000], gromiids [Burki et al. 2002], testate amoebae [Wylezich et al. 2002], filose and re-ticulate protists [Nikolaev et al. 2003], and radiolarians [Polet et al. 2004]. A strong support for Rhizaria, composed of all previously included taxonomic groups, plus Des-mothoracida and Taxopodida, was recovered in a combined analysis of actin and SSU rDNA genes [Nikolaev et al. 2004]. The rhizarian supergroup is growing continuously by new inclusions such as the marine flagellate ebriids [Hoppenrath and Leander 2006], the amoeboid Corallomyxa [Tekle et al. 2007], the parasitic plasmodial Paradinium [Skovgaard and Daugbjerg 2008] and the soil flagellate Sainouron [Cavalier-Smith et al.
E x c a v a t a: This supergroup is composed of diverse heterotrophic protists, many of which are anaerobic and/or parasitic, characterized by a distinctive feeding groove and two flagella in most, but not all, of these organisms [Simpson 2003]. It is tentatively as-sembled in one monophyletic entity by a combination of molecular and morphological data [Simpson 2003], but to date a robust evidence is still lacking, although a recent phylogenomic study recovered moderate support for this supergroup [Hampl et al.
The four supergroups described above are often known as the B i k o n t assemblages [Cavalier-Smith 2002].