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The impact of these factors on the rooting of a tree including Archaea, Asgard, and Eukarya have yet to be tested. A rooting congruent with earlier 3-Domain topologies remains plausible, and the implications thereof are important to consider, especially in light of character-based arguments for the unity of Asgard and Archaea made independently of phylogenetic evidence. ESPs black dots are synapomorphies uniting Asgard and eukaryotes as a clade gray bar. Additional archaeal groups e. Archaea are depicted as rooted between Euryarchaeota and TACK, although this hypothetical 3-Domain topology is also valid under all other rootings for this group.

Complete genome sequencing of members of the Asgard superphylum will allow this prediction to be tested. If Eukarya roots within extant archeal diversity, one can more clearly polarize the shared ancestral characters within Eukarya, and infer that the earliest stem eukaryotes were essentially archaeal, in both a systematic and physiological sense.

However, the same shared derived characters of ESPs would still unite Eukarya and Asgard, and their monophyly would still stand, albeit as a clade of a lower taxonomic rank than Archaea Figure 3. Note that the scenarios in Figures 2 , 3 only differ in the placement of the root, not in the topology of the tree or mapping of the characters. It is worth considering another parallel case from vertebrate evolution depicted in Figure 1 , that of the relationship between Aves birds and other reptilian lineages.

The extant sister group to birds, Crocodilia, retains several ancestral characters in common with other reptile outgroups, but also show derived characters linking them to birds within the wider group Archosauria, including their extinct relatives, pterosaurs and non-avian dinosaurs e.

Birds are excluded because of their highly derived set of characters that distinguish them morphologically, specifically, adaptations for flight. However, this is not a systematic criterion, and rather reflects a character-based distinction that is intuitively satisfying based on historical classification schemes. Extending the analogy to Archaea, in a similar case of a paraphyletic, 2-Domain tree, should Asgard still be grouped with Eukarya to the exclusion of Archaea, based on the monophyly of these groups and their associated synapomorphies?

The case would rest upon which derived characters were selected to exclude Eukarya and Asgard from Archaea, rendering the latter paraphyletic. An apomorphy-based definition would, in this case, be necessary to justify such paraphyly. If the evolutionary grade leading to Eukarya traversed a continuum of physiological and genetic innovations, selecting a single derived character defining this group to the exclusion of archaeal ancestors is not only challenging, but inherently problematic.

This is a general problem within taxonomy, and does not indicate that eukaryote evolution requires special consideration, or a re-evaluation of traditional cladistics principles. However, regardless of any apomorphy-based definition of Eukarya, Asgard and Eukarya would still represent a distinct clade within Archaea, defined by shared derived characters associated with the evolution of key eukaryote-like cytological features, and requiring taxonomic recognition.

The acquisition of the mitochondrial lineage is undoubtedly one of the most important evolutionary events in the history of life on Earth. This is a complex evolutionary narrative requiring numerous assumptions Lynch and Marinov, , and has been challenged by alternative models in which many of these same eukaryal-specific characters are required for the uptake and maintenance of the symbiont ancestors of the mitochondrial lineage Cavalier-Smith, ; Martijn and Ettema, ; Poole and Gribaldo, ; Pittis and Gabaldon, As some ESP proteins found within Asgard are orthologous to proteins in eukaryotes that are associated with vesicle formation, membrane trafficking, and cytoskeletal functions Spang et al.

Aside from these arguments, the following evolutionary thought experiments challenge the notion of a mitocentric view of eukaryal evolution, by addressing the metabolic, genetic, and cytological features of this event. The mitochondrial acquisition represents three specific changes to the eukaryal ancestor lineage, metabolic the acquisition of aerobic respiration , genetic the acquisition of a large number of bacterial genes , and cytological the maintenance of a highly derived replicating organelle.

The different aspects of this single event can, conceptually, be considered individually. If there had never been an endosymbiotic event giving rise to mitochondria, but the genes for aerobic respiration had nevertheless been acquired by horizontal gene transfer HGT from an alphaproteobacterial lineage, would this event, in itself, have the same weight as a defining character for Eukarya?

The wider domain of evolutionary thought (studies in history and phil…

Metabolic innovations, including aerobic respiration, often evolve via HGT across microbial lineages. The widespread distribution of aerobic respiration across the Tree of Life shows that this character would be a poor synapomorphy to define Eukarya as a distinct Domain of life. From a genetic perspective, many genes of bacterial origin were transferred as a consequence of the mitochondrial endosymbiotic event, although it is likely that many of the genes also shared between Eukarya and Bacteria were not necessarily acquired in this way, as they have evidence of different evolutionary histories Huang, Furthermore, a large influx of genetic information from a specific donor lineage is also frequently encountered in microbial groups [e.

This analogy also appears to hold for the mitochondrial lineage within Eukarya, where endosymbiotic gene transfer EGT began after mitochondria were acquired, likely in concert with mitochondrial genome reduction, and continued after the diversification of extant eukaryal groups in a clade-specific fashion, especially in plants Adams and Palmer, ; Bonen and Calixte, If the only difference between EGT and a highway of HGT is the symbiotic intermediary, it is arguable that this is not a meaningful distinction.

The acquisition of mitochondria is therefore most unique and distinct from archaeal and bacterial evolutionary processes from a cytological perspective. Obligate, co-evolved endosymbioses involving radical genome reduction are common among bacterial endosymbionts of eukaryotes McCutcheon, In contrast with these examples, it is the intimate integration of the mitochondria with both nuclear and cytosolic cellular components and processes that argue for their being a key character of Eukarya.

However, comparison with another endosymbiotic event within eukaryal evolution, the acquisition of a cyanobacterial endosymbiont establishing the plastid-containing eukaryal group Archaeplastida, provides valuable context for these claims. Yet, none of these evolutionary events and derived characters are elevated to the degree that Archaeplastida is argued to constitute a new Domain of life arising from within a paraphyletic Eukarya.

This comparison further reveals the problematic nature of a mitocentric view of eukaryal origins. Rather than focusing on this one character, it is more useful to consider stem eukaryotes as an evolutionary grade containing an ordered series of many complex derived characters, of which mitochondrial acquisition is merely one Poole and Gribaldo, Cladogram of Asgard and eukaryote evolution as related to different definitions of Eukarya.

An apomorphy-based definition of Eukarya requires the identification of a specific defining character for Eukarya, which would include some eukaryal stem groups, but exclude others. The selection of a defining character for an apomorphy-based definition is therefore inherently subjective. The Asgard group is depicted as an evolutionary grade, although a monophyletic Asgard group is also consistent with this model. Gene tree phylogenies tend to recover the monophyly of Eukarya and Asgard groups. ESPs have been identified in these newly discovered groups, reinforcing this proposed relationship.

We propose that these results are consistent with the interpretation that Eukarya and Asgard lineages form a distinct clade defined by shared derived characters. A correct application of cladistics requires grouping based on shared derived characters. Many ancestral archaeal-like characters were retained in the Asgard lineages, and these would have been present in the earliest direct stem Eukarya ancestors, as well. These ancestral characters are, in themselves, insufficient to define Asgard lineages as members of Archaea except in the sense that, under 2-Domain tree topologies, both Asgard and Eukarya are part of the archaeal tree.

Rather, the placement of the root leading to Bacteria provides this distinction. While current phylogenomic analyses favor a rooting within Archaea, this placement is highly sensitive to a variety of factors, and continues to be debated.

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Both 2-Domain and 3-Domain scenarios are compatible with treating Asgard lineages as members of a distinct and broader group including eukaryotes that requires taxonomic recognition. GF originated and devised the study, which was further developed in collaboration with AP. GF drafted the figures. GF and AP drafted the manuscript.

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The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Adams, K. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Beiko, R. Highways of gene sharing in prokaryotes. Benson, R. Interrelationships of basal synapsids: cranial and postcranial morphological partitions suggest different topologies.

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Kammerer, C. Klinger, C. Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Koonin, E.

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The origin and early evolution of eukaryotes in the light of phylogenomics. Genome Biol. Koumandou, V. Molecular paleontology and complexity in the last eukaryotic common ancestor.

Lasek-Nesselquist, E. The effects of model choice and mitigating bias on the ribosomal tree of life. Lynch, M. Membranes, energetics, and evolution across the prokaryote-eukaryote divide. Martijn, J.

The evolution (or diachrony) of “language evolution”

From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Martin, W. Introns and the origin of nucleus-cytosol compartmentalization. Nature , 41— McCutcheon, J. From microbiology to cell biology: when an intracellular bacterium becomes part of its host cell. Nasir, A. Arguments reinforcing the three-domain view of diversified cellular life. Each volume will comprise a group of essays on a connected theme, edited by an Australian or a New Zealander with special expertise in that particular area.

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Papers will address general issues; parochial topics will be avoided. JavaScript is currently disabled, this site works much better if you enable JavaScript in your browser. Buy eBook. Buy Hardcover. Buy Softcover. FAQ Policy. About this book Only in fairly recent years has History and Philosophy of Science been recognized - though not always under that name - as a distinct field of scholarly endeavour.

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