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On the need for integrative phylogenomics, and some steps toward its creation

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Abstract

Recently improved understanding of evolutionary processes suggests that tree-based phylogenetic analyses of evolutionary change cannot adequately explain the divergent evolutionary histories of a great many genes and gene complexes. In particular, genetic diversity in the genomes of prokaryotes, phages, and plasmids cannot be fit into classic tree-like models of evolution. These findings entail the need for fundamental reform of our understanding of molecular evolution and the need to devise alternative apparatus for integrated analysis of these genomes. We advocate the development of integrative phylogenomics for analyzing these genomes and their histories, with tools suited to analyzing the importance of lateral gene transfer (LGT) and of DNA evolution in extra-cellular mobile genetic elements (e.g., viruses, plasmids). These phenomena greatly increase the complexity of relationships among interacting genetic partners, as they exchange functional genetic units. We examine the ontology of functional genetic units, interacting genetic partners, and emergent genetic associations, argue that these three categories of entities are required for a successful integrated phylogenomics. We conclude with arguments to suggest that the proposed new perspective and associated tools are suitable, and perhaps required, as a replacement for the bifurcating trees that have dominated evolutionary thinking for the last 150 years.

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Notes

  1. The degree of similarity between the trees depends on the extent of lateral transfer in the lineage of cells or organisms in question; occasionally such evidence indicates that particular groups of genes have distinct evolutionary histories from those of other groups of genes in the organism.

  2. There can be a hierarchical structure in such a network, but it can only be inferred using computationally demanding methods. There is no a priori reason for such a hierarchy to reflect the genealogy.

  3. These operational taxonomic units were described by Sneath and Sokal to give a rank-free name to the leaves of a phylogenetic tree (Sneath and Sokal 1973). Interpreted thus, molecular OTUs are representative of species, genera, individuals, and so on. Such OTUs have been used extensively to construct phylograms and maximum likelihood trees. One result of this use is that ‘OTU’ is now-standard term in molecular phylogenetics for leaves (or terminal taxa) on a tree.

  4. ‘Assortative’ is a term for networks in which partners with many connections connect preferentially with each other, rather than with partners with few interactions.

  5. Identification of genetic complexes inherited or transferred as a unit does not suffice to determine their evolutionary fate. Whether they achieve (or have achieved) the status of being a causally relevant evolutionary unit requires a diachronic analysis, which no synchronic categorization, by itself, can provide.

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Acknowledgments

We thank the “Questioning the Tree of Life” project, sponsored by the Leverhulme Trust, for encouraging this contribution. EB thanks J. Leigh, P. Lopez, S. Halary, F.J. ‘Quick’ Lapointe and Y. Boucher for stimulating discussions; RB thanks J. Jelesko, R. Jensen, B. Mukhopadhyay, and J. Sebutal for stimulating discussions.

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  1. UMR CNRS 7138, UPMC, 7, Quai Saint Bernard, 75005, Paris, France

    Eric Bapteste

  2. Department of Philosophy – 0126, Virginia Tech, Blacksburg, VA, 24061, USA

    Richard M. Burian

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Correspondence to Eric Bapteste.

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This paper has its roots in the fertile research fields masterfully sown by Ford Doolittle.

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Bapteste, E., Burian, R.M. On the need for integrative phylogenomics, and some steps toward its creation. Biol Philos 25, 711–736 (2010). https://doi.org/10.1007/s10539-010-9218-2

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