Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex

Conflict and cooperation in eukaryogenesis: implications for the timing of endosymbiosis and the evolution of sex
Arunas L Radzvilavicius, Neil W Blackstone
doi: http://dx.doi.org/10.1101/023077

The complex eukaryotic cell is a result of an ancient endosymbiosis and one of the major evolutionary transitions. The timing of key eukaryotic innovations relative to the acquisition of mitochondria remains subject to considerable debate, yet the evolutionary process itself might constrain the order of these events. Endosymbiosis entailed levels-of-selection conflicts, and mechanisms of conflict mediation had to evolve for eukaryogenesis to proceed. The initial mechanisms of conflict mediation were based on the pathways inherited from prokaryotic symbionts and led to metabolic homeostasis in the eukaryotic cell, while later mechanisms (e.g., mitochondrial gene transfer) contributed to the expansion of the eukaryotic genome. Perhaps the greatest opportunity for conflict arose with the emergence of sex involving whole-cell fusion. While early evolution of cell fusion may have affected symbiont acquisition, sex together with the competitive symbiont behaviour would have destabilised the emerging higher-level unit. Cytoplasmic mixing, on the other hand, would have been beneficial for selfish endosymbionts, capable of using their own metabolism to manipulate the life history of the host. Given the results of our mathematical modelling, we argue that sex represents a rather late proto- eukaryotic innovation, allowing for the growth of the chimeric nucleus and contributing to the successful completion of the evolutionary transition.

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