The evolution of sex: A new hypothesis based on mitochondrial mutational erosion

Havird, Justin C.; Hall, Matthew D.; Dowling, Damian K.

doi:10.1002/bies.201500057

Cited by 57 publications

(53 citation statements)

References 97 publications

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“…Views on the origin of sex have not changed at the same pace, though there is increasing interest in the possible role(s) of mitochondria in promoting the establishment of meiotic recombination (Lane 2009,2015; Speijer et al 2015; Havird et al 2015; Radzvilavicius and Blackstone 2015). Here, we have considered the origin of sex on the basis of those newer premises.…”

Section: Resultsmentioning

confidence: 99%

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Garg

Martin

2016

Genome Biol Evol

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Theories for the origin of sex traditionally start with an asexual mitosing cell and add recombination, thereby deriving meiosis from mitosis. Though sex was clearly present in the eukaryote common ancestor, the order of events linking the origin of sex and the origin of mitosis is unknown. Here, we present an evolutionary inference for the origin of sex starting with a bacterial ancestor of mitochondria in the cytosol of its archaeal host. We posit that symbiotic association led to the origin of mitochondria and gene transfer to host’s genome, generating a nucleus and a dedicated translational compartment, the eukaryotic cytosol, in which—by virtue of mitochondria—metabolic energy was not limiting. Spontaneous protein aggregation (monomer polymerization) and Adenosine Tri-phosphate (ATP)-dependent macromolecular movement in the cytosol thereby became selectable, giving rise to continuous microtubule-dependent chromosome separation (reduction division). We propose that eukaryotic chromosome division arose in a filamentous, syncytial, multinucleated ancestor, in which nuclei with insufficient chromosome numbers could complement each other through mRNA in the cytosol and generate new chromosome combinations through karyogamy. A syncytial (or coenocytic, a synonym) eukaryote ancestor, or Coeca, would account for the observation that the process of eukaryotic chromosome separation is more conserved than the process of eukaryotic cell division. The first progeny of such a syncytial ancestor were likely equivalent to meiospores, released into the environment by the host’s vesicle secretion machinery. The natural ability of archaea (the host) to fuse and recombine brought forth reciprocal recombination among fusing (syngamy and karyogamy) progeny—sex—in an ancestrally meiotic cell cycle, from which the simpler haploid and diploid mitotic cell cycles arose. The origin of eukaryotes was the origin of vertical lineage inheritance, and sex was required to keep vertically evolving lineages viable by rescuing the incipient eukaryotic lineage from Muller’s ratchet. The origin of mitochondria was, in this view, the decisive incident that precipitated symbiosis-specific cell biological problems, the solutions to which were the salient features that distinguish eukaryotes from prokaryotes: A nuclear membrane, energetically affordable ATP-dependent protein–protein interactions in the cytosol, and a cell cycle involving reduction division and reciprocal recombination (sex).

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Section: Resultsmentioning

confidence: 99%

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Garg

Martin

2016

Genome Biol Evol

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“…Mitonuclear interactions have been theorized to have important implications for human health, diversification of eukaryotes, and major transitions in the evolution of life (Burton and Barreto 2012; Dowling 2014; Havird et al. 2015a; Hill 2015; Sloan et al.…”

Section: Discussionmentioning

confidence: 99%

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

Havird

Trapp

Miller

et al. 2017

Genome Biology and Evolution

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Understanding mechanisms of coevolution between nuclear and mitochondrial (mt) genomes is a defining challenge in eukaryotic genetics. The angiosperm genus Silene is a natural system to investigate the causes and consequences of mt mutation rate variation because closely related species have highly divergent rates. In Silene species with fast-evolving mtDNA, nuclear genes that encode mitochondrially targeted proteins (N-mt genes) are also fast-evolving. This correlation could indicate positive selection to compensate for mt mutations, but might also result from a recent relaxation of selection. To differentiate between these interpretations, we used phylogenetic and population-genetic methods to test for positive and relaxed selection in three classes of N-mt genes (oxidative phosphorylation genes, ribosomal genes, and “RRR” genes involved in mtDNA recombination, replication, and repair). In all three classes, we found that species with fast-evolving mtDNA had: 1) elevated dN/dS, 2) an excess of nonsynonymous divergence relative to levels of intraspecific polymorphism, which is a signature of positive selection, and 3) no clear signals of relaxed selection. “Control” genes exhibited comparatively few signs of positive selection. These results suggest that high mt mutation rates can create selection on N-mt genes and that relaxed selection is an unlikely cause of recent accelerations in the evolution of N-mt genes. Because mt-RRR genes were found to be under positive selection, it is unlikely that elevated mt mutation rates in Silene were caused by inactivation of these mt-RRR genes. Therefore, the causes of extreme increases in angiosperm mt mutation rates remain uncertain.

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“…Interface 12: 20150584 be established before it was safe enough to engage in sexual reproduction and cytoplasmic mixing. Traditionally, the evolution of sex has been analysed in the context of recombination among nuclear genes and DNA repair, with only a few recent exceptions (notably [46]). It is not clear, however, whether the same evolutionary forces were responsible for the origin of between-host fusion during the eukaryogenesis, when the higher-level unit was still emerging.…”

Section: Discussionmentioning

confidence: 99%

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

Radzvilavicius

Blackstone

2015

J. R. Soc. Interface.

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Roughly 1.5-2.0 Gya, the eukaryotic cell evolved from an endosymbiosis of an archaeal host and proteobacterial symbionts. The timing of this endosymbiosis relative to the evolution of eukaryotic features remains subject to considerable debate, yet the evolutionary process itself constrains the timing 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 (e.g. signalling with calcium and soluble adenylyl cyclase, substrate carriers, adenine nucleotide translocase, uncouplers) led to metabolic homeostasis in the eukaryotic cell. Later mechanisms (e.g. mitochondrial gene loss) contributed to the chimeric eukaryotic genome. These integral features of eukaryotes were derived because of, and therefore subsequent to, endosymbiosis. Perhaps the greatest opportunity for conflict arose with the emergence of eukaryotic sex, involving whole-cell fusion. A simple model demonstrates that competition on the lower level severely hinders the evolution of sex. Cytoplasmic mixing, however, is beneficial for non-cooperative endosymbionts, which could have used their aerobic metabolism to manipulate the life history of the host. While early evolution of sex may have facilitated symbiont acquisition, sex would have also destabilized the subsequent endosymbiosis. More plausibly, the evolution of sex and the true nucleus concluded the transition.

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The evolution of sex: A new hypothesis based on mitochondrial mutational erosion

Cited by 57 publications

References 97 publications

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Mitochondria, the Cell Cycle, and the Origin of Sex via a Syncytial Eukaryote Common Ancestor

Causes and Consequences of Rapidly Evolving mtDNA in a Plant Lineage

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

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