Radzvilavicius, A;
(2017)
Evolutionary Dynamics Of Mitochondrial Mutations In The Origin And Development Of Eukaryotic Sex.
Doctoral thesis , UCL (University College London).
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Abstract
Sexual reproduction is virtually universal among eukaryotes, suggesting that the last eukaryotic common ancestor was already sexual. It is very likely that the first sexual lineage already contained mitochondrial endosymbionts, each with its own genome of bacterial origin. In this thesis I develop a set of theoretical models that together form a framework for understanding the evolution of eukaryotic sex and further sexual traits— mating types, uniparental inheritance, sexual dimorphism and the early sequestration of a protected germline in higher metazoans—as a consequence of mitochondrial endosymbiosis. First, I review currently dominating views on the origin of eukaryotes and selective forces that led to the evolution of meiotic sex early in the prokaryote- eukaryote transition. Sex likely emerged as a direct consequence of the mitochondrial endosymbiosis, and was essential for the further evolution of eukaryotic genome complexity. In Chapter 2, I show that the evolution of sexual cell fusion in the nascent eukaryotic lineage might have been driven by cytoplasmic mixing, temporarily masking the detrimental effects of defective organelles. The model introduced in Chapter 3 shows that self-incompatible mating types can evolve to ensure the efficient removal of mitochondrial mutations through asymmetric organelle transmission. Frequent observations of paternal leakage and heteroplasmy pose a substantial challenge to the current understanding of uniparental organelle inheritance. In Chapter 4 I show that the evolutionarily stable pattern of cytoplasmic inheritance depends on which sex—male or female—governs the destruction of paternal organelles. Maternal regulation favours complete elimination of sperm mitochondria, while paternal control supports paternal leakage and heteroplasmy. Intersexual competition over the control of cytoplasmic inheritance may have driven the repeated evolution of mechanisms enforcing uniparental inheritance. Finally, I analyse the dynamics of mitochondrial mutation segregation in the evolution of the metazoan germline. High mitochondrial DNA replication error rates in bilaterians favour early germline sequestration, while in basal metazoans gamete quality is maximized through repeated cell divisions in non-sequestered germline stem cell lineages.
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