Downloaded from rstb.royalsocietypublishing.org on July 31, 2010 Deep phylogeny, ancestral groups and the four ages of life Thomas Cavalier-Smith Phil. Trans. R. Soc. B 2010 365, 111-132 doi: 10.1098/rstb.2009.0161 References This article cites 73 articles, 28 of which can be accessed free http://rstb.royalsocietypublishing.org/content/365/1537/111.full.html#ref-list-1 Article cited in: http://rstb.royalsocietypublishing.org/content/365/1537/111.full.html#related-urls This article is free to access Rapid response Respond to this article http://rstb.royalsocietypublishing.org/letters/submit/royptb;365/1537/111 Subject collections Articles on similar topics can be found in the following collections evolution (1878 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Phil. Trans. R. Soc. B go to: http://rstb.royalsocietypublishing.org/subscriptions This journal is © 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on July 31, 2010 Phil. Trans. R. Soc. B (2010) 365, 111–132 doi:10.1098/rstb.2009.0161 Review Deep phylogeny, ancestral groups and the four ages of life Thomas Cavalier-Smith* Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Organismal phylogeny depends on cell division, stasis, mutational divergence, cell mergers (by sex or symbiogenesis), lateral gene transfer and death. The tree of life is a useful metaphor for organis- mal genealogical history provided we recognize that branches sometimes fuse. Hennigian cladistics emphasizes only lineage splitting, ignoring most other major phylogenetic processes. Though methodologically useful it has been conceptually confusing and harmed taxonomy, especially in mistakenly opposing ancestral (paraphyletic) taxa. The history of life involved about 10 really major innovations in cell structure. In membrane topology, there were five successive kinds of cell: (i) negibacteria, with two bounding membranes, (ii) unibacteria, with one bounding and no internal membranes, (iii) eukaryotes with endomembranes and mitochondria, (iv) plants with chloroplasts and (v) finally, chromists with plastids inside the rough endoplasmic reticulum. Membrane chemistry divides negibacteria into the more advanced Glycobacteria (e.g. Cyanobac- teria and Proteobacteria) with outer membrane lipolysaccharide and primitive Eobacteria without lipopolysaccharide (deserving intenser study). It also divides unibacteria into posibacteria, ancestors of eukaryotes, and archaebacteria—the sisters (not ancestors) of eukaryotes and the youngest bacterial phylum. Anaerobic eobacteria, oxygenic cyanobacteria, desiccation-resistant posibacteria and finally neomura (eukaryotes plus archaebacteria) successively transformed Earth. Accidents and organizational constraints are as important as adaptiveness in body plan evolution. Keywords: bacteria; protozoa; symbiogenesis; kingdoms of life; lateral gene transfer; classification 1. INTRODUCTION Hennig’s (1966) ‘phylogenetic systematics’, often The nature of the deepest branches in the evolutionary accompanied by much controversy. Great advances tree and the last common ancestor of all life are key in knowledge and understanding of organismal history questions in biology having wide ramifications. Cur- have been made, but some fashions, attitudes and rently, we are in the early stages of a paradigm shift dogmas have spread more widely and dominated in which the prevailing view on these matters should other viewpoints more than their scientific merits jus- be replaced by a sounder one. This review summarizes tify. The significance of the stasis of ancestral body recent insights into bacterial and protozoan large-scale plans over billenia and the non-uniformity of evol- evolution and the tree of life for non-specialists and utionary modes and rates is insufficiently argues that much more intense research into the appreciated. Much discussion has been among stu- little-known phylum Chlorobacteria is needed for dents of recently derived branches of the tree better understanding the nature of our last common (Hennig insects; Mayr birds) or among those whose ancestor. To avoid burdening you with excessive focus is biochemistry or computer algorithms, rather detail, I do this rather briefly in the second half of than organisms and the needs and principles of taxon- this essay, giving references to specialist literature for omy. I offer the perspective of a biologist especially those wanting more detail or evidence for my interested in unicellular organisms, ancestral groups conclusions. and in explaining the major transitions of life, perhaps The first half is a broader historical/philosophical more conscious than most of flaws in some aspects of discussion of the contrast between ancestral and recent phylogenetic fashions. derived groups and how taxonomists should handle Soon after it was founded, the Royal Society them. The past three decades have seen a dramatic published Micrographia in which Hooke (1664) increase in the use of DNA sequences for reconstruct- applied the word cell for the first time to the walled ing phylogeny and a parallel shift in emphasis units of dead plant tissues that he first depicted. from evolutionary taxonomy (Mayr 1974) towards However, the modern concept of cells as living units that multiply by division grew up only in the mid nine- teenth century simultaneously with that of evolution *[email protected] by variation and selection. Weismann (1889) made One contribution of 19 to a Theme Issue ‘Personal perspectives in the first synthesis of cell biology and evolution, in the life sciences for the Royal Society’s 350th anniversary’. which cell lineages were seen as the physical basis for 111 This journal is q 2010 The Royal Society Downloaded from rstb.royalsocietypublishing.org on July 31, 2010 112 T. Cavalier-Smith Review. Phylogeny, ancestral groups & early life inheritance and evolution, but his emphasis was all on dictum was ‘publish and perish’. Chambers wrote nucleated cells, as was Wallace’s (1911) claim that only well after the Pope banned Zoonomia by Charles a creative mind could have made them. Understanding Darwin’s grandfather Erasmus, who first correctly the big picture of organismal history requires more suggested that all organisms evolved by modifying a attention than hitherto to the main features of the single microbial common ancestor (Darwin 1794), evolution of sexless bacterial cells which exclusively but during the British backlash against progressive dominated the biosphere for three-quarters of its ideas, especially foreign French ones like those of history. More than all eukaryotes together, bacteria de Maupertuis, De Maillet and Lamarck (1809). still largely manipulate biogeochemical cycles and Lamarck in French and Chambers in English first global climate. proposed phylogenetic trees for real organisms. Darwin Though I shall not dwell on it, another limitation of (1859) scrupulously avoided doing that. Unmerited Weismann’s synthesis has become apparent in the past ridicule as they suffered would have jeopardized his two decades. Superimposed on the vertical inheritance threefold mission: demonstrating the fact of evolution; of cell lineages that Weismann recognized is the hori- showing how the struggle for existence explains adap- zontal transfer of individual genes or small clusters of tation; and attempting to explain evolutionary change genes among organisms of separate cell lineages, (transformation) by genetic variation and the differential which can affect the evolution of extremely distantly multiplication of genotypes. When emphasizing how related organisms. In bacteria, such lateral gene common ancestry plus divergence into novel phenotypes transfer (LGT) occurs mainly by viruses, plasmids or explain the striking patterns of similarity and differences the uptake of naked DNA from dead cells. In eukar- that enable us to classify organisms into successively yotes, feeding by phagocytosis followed by inefficient nested taxa within higher taxa, Darwin cleverly used an digestion of prey DNA and its accidental incorporation abstract tree immune to ridicule or phylogenetic error. into nuclear chromosomes is probably how protozoa He correctly argued that the body plan shared by mem- most often get foreign genes (Doolittle 1998). bers of a phylum was present in their last common Although LGT of DNA independently of cell lineages ancestor and has been stably inherited generation after is evolutionarily important, especially among bacteria generation, with no fundamental change for hundreds and protozoa (see Cavalier-Smith submitted a), it of millions of years. Proceeding down the hierarchy of seems to have played no role in the evolution of the categories through class, order, family, genus and major cellular body plans that I focus on here. species, each successive subordinate group differs from its closest relatives in characters of decreasing long-term stability (Lamarck 1809). 2. EARLY PERCEPTIONS OF CELL LINEAGES Chambers wrote shortly after Meyen (1839), AND THE UNITY OF LIFE Dujardin (1841) and Barry (1843) unified biology by showing that protozoa are single nucleated cells hom- Shall we conjecture that one and the same kind of living ologous with those forming animal and plant bodies filaments is and has been the cause of all organic life? and that continuous cell lineages are the physical (Darwin 1794, p. 507) basis of life. (The