The impact of history on our perception of evolutionary events: endosymbiosis and the origin of eukaryotic complexity

Abstract

Evolutionary hypotheses are correctly interpreted as products of the data they set out to explain, but they are less often recognized as being heavily influenced by other factors. One of these is the history of preceding thought, and here I look back on historically important changes in our thinking about the role of endosymbiosis in the origin of eukaryotic cells. Specifically, the modern emphasis on endosymbiotic explanations for numerous eukaryotic features, including the cell itself (the so-called chimeric hypotheses), can be seen not only as resulting from the advent of molecular and genomic data, but also from the intellectual acceptance of the endosymbiotic origin of mitochondria and plastids. This transformative idea may have unduly affected how other aspects of the eukaryotic cell are explained, in effect priming us to accept endosymbiotic explanations for endogenous processes. Molecular and genomic data, which were originally harnessed to answer questions about cell evolution, now so dominate our thinking that they largely define the question, and the original questions about how eukaryotic cellular architecture evolved have been neglected. This is unfortunate because, as Roger Stanier pointed out, these cellular changes represent life's "greatest single evolutionary discontinuity," and on this basis I advocate a return to emphasizing evolutionary cell biology when thinking about the origin of eukaryotes, and suggest that endogenous explanations will prevail when we refocus on the evolution of the cell.

Figure 1.

Distribution of character states between three domains on the tree of life and how we interpret them. When Bacteria and Archaea share a state and eukaryotes are different (type E), we typically conclude that the shared state is ancestral to the LUCA and eukaryotes changed. When eukaryotes and Archaea share a state and Bacteria are unique (type B), we similarly conclude that the shared state was ancestral to the LECA, and either Bacteria or the lineage leading to the LECA changed. But when Bacteria and eukaryotes share a state and Archaea are unique (type A), we seem to have trouble applying the same logic, which would at face value simply be to conclude that the shared state was ancestral to the LUCA and that Archaea had changed.