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TRENDS in Genetics Vol.20 No.4 April 2004

Cladogenesis, coalescence and the evolution of the three domains of life
Olga Zhaxybayeva and J. Peter Gogarten
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA

In this article, we explore the large-scale structure of the tree of life by using a simple model with a constant number of species andrates of speciation that equal the rates of extinction. In addition, we discuss the consequences of horizontal gene transfer for the concept of a most recent common ancestor of all living organisms (cenancestor). A simple null hypothesis based on coalescence theory explains some features of the observed topologies of the tree of life. Simulations of genes and organismal lineages suggest thatthere was no single common ancestor that contained all the genes ancestral to those shared among the three domains of life. Each contemporary molecule has its own history that traces back to an individual molecular cenancestor. However, these molecular ancestors were likely to be present in different organisms and at different times. The tracing and timing of the most recent common ancestor of allorganismal lineages [i.e. CENANCESTOR (see Glossary)] from the molecular record remains one of the debated issues in biology. Since Charles Darwin’s time it has been assumed that there was a single organism that gave rise to all known life. With the availability of many molecular markers, it became clear that different molecules have different histories and there is disagreement on the location ofthe root of the tree of life (e.g. different studies place the root: (i) within the bacterial domain or on the branch that leads to the bacterial domain [1,2]; (ii) within the eukaryotic domain [3– 5]; (iii) within the archaeal domain [6]; or (iv) yield inconclusive results [7]). The timing of the organismal cenancestor is another unresolved question [8 –11]. The time estimates vary dramatically,and in many instances the proposed age of the most recent common ancestor exceeds the estimated age of the Universe ([12] and J.P. Gogarten, unpublished). The probable absence of an adequate amount of time for life to evolve on Earth is used by the proponents of the directed panspermia hypothesis [13], which states that life originated elsewhere and was deliberately transported to Earth. Tracingback the history of molecules usually reveals little about extinct lineages. Reconstructed phylogenies, because of their steadily furcating nature, often give the impression that there were fewer species in the past than exist today. Many analyses only focus on the ‘lucky ancestors’ whose offspring survived to the present
Corresponding author: J. Peter Gogarten (

day (or lefta recognizable imprint in the fossil record). However, it is reasonable to assume that in addition to these ‘lucky ancestors’ there were many other lineages that coexisted in the past and occupied all ecological niches that were available: most of those lineages became extinct, some gave rise to new lineages, some fused with others and some have contributed genes via horizontal gene transfer (HGT)to the lineages that still exist today. As lineages coalesce to their common ancestors, they form clades. The rate of cladogenesis is an interesting problem [14]. How often do new clades arise? Is the extinction rate equal to the speciation rate? What are the driving forces for cladogenesis? Several authors have described mathematical models for cladogenesis [15,16] and goodness-of-fit tests toascertain if models accurately explain the data [17,18], and have attempted to infer extinction and speciation rates from phylogenetic trees [18,19]. Two simple models of cladogenesis can be used as null hypotheses: (i) a pure-birth model (i.e. a model based
Cenancestor: from the Greek ‘kainos’ meaning recent and ‘koinos’ meaning common – the most recent common ancestor of all the...
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