Gene sharing and genome evolution: networks in trees and trees in networks

Abstract

Frequent lateral genetic transfer undermines the existence of a unique “tree of life” that relates all organisms. Vertical inheritance is nonetheless of vital interest in the study of microbial evolution, and knowing the “tree of cells” can yield insights into ecological continuity, the rates of change of different cellular characters, and the evolutionary plasticity of genomes. Notwithstanding within-species recombination, the relationships most frequently recovered from genomic data at shallow to moderate taxonomic depths are likely to reflect cellular inheritance. At the same time, it is clear that several types of ‘average signals’ from whole genomes can be highly misleading, and the existence of a central tendency must not be taken as prima facie evidence of vertical descent. Phylogenetic networks offer an attractive solution, since they can be formulated in ways that mitigate the misleading aspects of hybrid evolutionary signals in genomes. But the connections in a network typically show genetic relatedness without distinguishing between vertical and lateral inheritance of genetic material. The solution may lie in a compromise between strict tree-thinking and network paradigms: build a phylogenetic network, but identify the set of connections in the network that are potentially due to vertical descent. Even if a single tree cannot be unambiguously identified, choosing a subnetwork of putative vertical connections can still lead to drastic reductions in the set of candidate vertical hypotheses.