Evolutionary analyses of non-genealogical bonds produced by introgressive descent

Abstract

All evolutionary biologists are familiar with evolutionary units that evolve by vertical descent in a tree-like fashion in single lineages. However, many other kinds of processes contribute to evolutionary diversity. In vertical descent, the genetic material of a particular evolutionary unit is propagated by replication inside its own lineage. In what we call introgressive descent, the genetic material of a particular evolutionary unit propagates into different host structures and is replicated within these host structures. Thus, introgressive descent generates a variety of evolutionary units and leaves recognizable patterns in resemblance networks. We characterize six kinds of evolutionary units, of which five involve mosaic lineages generated by introgressive descent. To facilitate detection of these units in resemblance networks, we introduce terminology based on two notions, P3s (subgraphs of three nodes: A, B, and C) and mosaic P3s, and suggest an apparatus for systematic detection of introgressive descent. Mosaic P3s correspond to a distinct type of evolutionary bond that is orthogonal to the bonds of kinship and genealogy usually examined by evolutionary biologists. We argue that recognition of these evolutionary bonds stimulates radical rethinking of key questions in evolutionary biology (e.g., the relations among evolutionary players in very early phases of evolutionary history, the origin and emergence of novelties, and the production of new lineages). This line of research will expand the study of biological complexity beyond the usual genealogical bonds, revealing additional sources of biodiversity. It provides an important step to a more realistic pluralist treatment of evolutionary complexity.

Fig. 1.

Selection of gene network components displaying their largest maximal clique. Genes (nodes; in gray) aligning >80% of their sequences with their match in a BLAST analysis (showing >50% identification and a BLAST score < 1 e⁻²⁰) are directly connected. Sequences belonging to the largest maximal clique, defining the largest set easily amenable for a single phylogenetic analysis, are highlighted in bright colors. The largest maximal clique only covers a portion of each component, meaning that numerous similarity relationships and evolutionary relationships cannot be investigated using a single tree. A corresponds to the Holin BlyA family (only plasmids; 87 nodes in the clique). B contains AC3 and replication enhancer proteins (only viruses; 140 nodes in the clique). C corresponds to transposases OrfB family (mostly plasmids and a few prokaryotes; 50 nodes in the clique). D corresponds to oligopeptide ABC transporter ATP-binding proteins (mostly prokaryotes and some plasmids; 38 nodes in the clique).

Fig. 2.

Patterns with evolutionary significance in resemblance networks. Each symbol indicates an entity (node) from a distinct level of biological organization. Similarly colored edges indicate vertically inherited shared characters. Occurrences in our test dataset at >50% identification are quantified when available. (A) Clique (here, a triangle) capturing a homology relationship between A, B, and C. (B) P3 occurring when a homologous character evolved beyond recognition between A and C. (C) M-P3 indirectly connecting two entities through a third one by different (pink and green) shared characters. (D) Multilevel M-P3 indicating multilevel evolutionary units. (E) Polarized M-P3 showing B as a merger or as a fissioning unit. (F) Pn (here, four). (G) Pn with the distantly related parts from a merger entity A. (H) Hardly detectable M-P3s. (Left) Ancient core characters mask a recent combination of characters in B. (Center) Real numbers of shared gene families between domains of life. (Right) Aggregation of three M-P3s looking like a clique. (I) Multilevel cliques.