Pattern pluralism and the Tree of Life hypothesis

Abstract

Darwin claimed that a unique inclusively hierarchical pattern of relationships between all organisms based on their similarities and differences [the Tree of Life (TOL)] was a fact of nature, for which evolution, and in particular a branching process of descent with modification, was the explanation. However, there is no independent evidence that the natural order is an inclusive hierarchy, and incorporation of prokaryotes into the TOL is especially problematic. The only data sets from which we might construct a universal hierarchy including prokaryotes, the sequences of genes, often disagree and can seldom be proven to agree. Hierarchical structure can always be imposed on or extracted from such data sets by algorithms designed to do so, but at its base the universal TOL rests on an unproven assumption about pattern that, given what we know about process, is unlikely to be broadly true. This is not to say that similarities and differences between organisms are not to be accounted for by evolutionary mechanisms, but descent with modification is only one of these mechanisms, and a single tree-like pattern is not the necessary (or expected) result of their collective operation. Pattern pluralism (the recognition that different evolutionary models and representations of relationships will be appropriate, and true, for different taxa or at different scales or for different purposes) is an attractive alternative to the quixotic pursuit of a single true TOL.

Fig. 1.

Two analogies to illustrate misapplication of tree-thinking. (A) Shown is a genealogy relating the senior author to another molecular evolutionist, Russell F. Doolittle. This pattern reflects the inheritance of surnames and Y chromosomes, but of <0.5% of our respective genomes. Only an extreme patriarchalist would privilege this particular pattern of relationships or the common ancestor we share over the hundreds that we do not so far back in history. And yet, such privileging is not dissimilar to basing the phylogeny of prokaryotes on only a tiny subset of the genes that any of them contain, knowing that other genes will give different results. (B) Shown is a second thought experiment, a distance tree of the départements of France based on the number of shared surnames (among the top 500) in pairwise comparisons of lists of the most frequent names in each. The pattern is interesting, tells us much about French history and demographics, and is ultimately based on the genealogies of individuals. Some of its nodes would likely also be recovered by independent measures, such as geographical separation or dietary preferences. But this pattern is by no means a phylogeny of French départements, because départements do not arise by a branching process of descent with modification and the nodes on this tree in no way correspond to ancestral departments. Yet similar trees based on shared gene content of genomes (even when extensive LGT is admitted) have often been presented as the phylogenies of those genomes, and the recovery of some nodes by independent measures (rRNA phylogenies) has been claimed in their support.