Furcation and fusion: The phylogenetics of evolutionary novelty

Abstract

Novelty and innovation are fundamental yet relatively understudied concepts in evolution. We may study the history and provenance of novelty using phylogenetics, where key questions include when evolution occurs by tree-like branching and when it occurs by movement of distantly related parts in processes akin to horizontal transfer. Perfectly vertical inheritance, often an assumption of evolutionary trees, requires simultaneous co-duplication of the parts of a duplicating or speciating (processes I collectively call 'furcating') biological feature. However, simultaneous co-duplication of many parts usually requires variational processes that are rare. Therefore, instead of always being perfectly tree-like, evolution often involves events that incorporate or fuse more distantly related parts into new units during evolution, which herein I call 'fusion'. Exon shuffling, horizontal gene transfer, introgression, and co-option are such fusion processes at different levels of organization. The ubiquity of processes that fuse distantly related parts has wide ranging implications for the study of macroevolution. For one, the central metaphor of a tree of life will often be incomplete, to the point where we may consider a different metaphor, such as economic public goods, or a 'web of life'. Secondly, we often may need to expand commonly used phylogenetic models and methods, highlighting a need for an expansive toolkit for studying evolutionary history. Even though furcation - the splitting and individuation of biological features - does happen, fusion of distant parts may often be just as critical for the evolution of novelties, and must formally be incorporated into the metaphors, models, and visualization of evolutionary history. This will allow us to understand the timing, order of appearance, and diversification rates of developmental systems, including cell types, organs, behavior, and language, which very commonly evolve through co-option.

Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts

“…Our data suggest that nearly half of the genes encoding pcwdCAZymes have been obtained by LGT from other fungi. Gene duplication, which has been described as a major source of gene innovation in fungi [ 67 ] and other organisms [ 68 ] apparently played only a minor role in the evolution of the Trichoderma pcwdCAZome. It has been reported that 0.1–3% of the genes in a given Pezizomycotina genome were derived by LGT, usually indicating interdomain exchanges [ 43 , 67 ].…”

Testing Finch's hypothesis: The role of organismal modularity on the escape from actuarial senescence

“…Evolutionarily, the configuration of developmental control genes may influence the development of accessory organs (Oakley, 2017).…”

Prospects for a General Theory of Evolutionary Novelty

“…For example, among Metazoa, four classes of genomic novelty have been recognized (Simakov and Kawashima, 2017), distinguished by the extent of sequence similarity and gene architecture (including domain order). Many novelties, at a variety of levels, occur through combinations of previously separate elements, ranging from the origin of the eukaryotic cell to co-option of regulatory subcircuits and fusion of different genes (see also Oakley, 2017).…”