title: Selection for Mitochondrial Quality Drives Evolution of the Germline.
abstract: The origin of the germline-soma distinction is a fundamental unsolved question. Plants and basal metazoans do not have a germline but generate gametes from pluripotent stem cells in somatic tissues (somatic gametogenesis). In contrast, most bilaterians sequester a dedicated germline early in development. We develop an evolutionary model which shows that selection for mitochondrial quality drives germline evolution. In organisms with low mitochondrial replication error rates, segregation of mutations over multiple cell divisions generates variation, allowing selection to optimize gamete quality through somatic gametogenesis. Higher mutation rates promote early germline sequestration. We also consider how oogamy (a large female gamete packed with mitochondria) alters selection on the germline. Oogamy is beneficial as it reduces mitochondrial segregation in early development, improving adult fitness by restricting variation between tissues. But it also limits variation between early-sequestered oocytes, undermining gamete quality. Oocyte variation is restored through proliferation of germline cells, producing more germ cells than strictly needed, explaining the random culling (atresia) of precursor cells in bilaterians. Unlike other models of germline evolution, selection for mitochondrial quality can explain the stability of somatic gametogenesis in plants and basal metazoans, the evolution of oogamy in all plants and animals with tissue differentiation, and the mutational forces driving early germline sequestration in active bilaterians. The origins of predation in motile bilaterians in the Cambrian explosion is likely to have increased rates of tissue turnover and mitochondrial replication errors, in turn driving germline evolution and the emergence of complex developmental processes.
authors.affiliation: Centre for Mathematics and Physics in the Life Sciences and Experimental Biology, University College London, London, United Kingdom.|Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors.forename: Arunas L
authors.initials: AL
authors.lastname: Radzvilavicius
authors.affiliation: Centre for Mathematics and Physics in the Life Sciences and Experimental Biology, University College London, London, United Kingdom.|Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors.forename: Zena
authors.initials: Z
authors.lastname: Hadjivasiliou
authors.affiliation: Centre for Mathematics and Physics in the Life Sciences and Experimental Biology, University College London, London, United Kingdom.|Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors.forename: Andrew
authors.initials: A
authors.lastname: Pomiankowski
authors.affiliation: Centre for Mathematics and Physics in the Life Sciences and Experimental Biology, University College London, London, United Kingdom.|Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom.
authors.forename: Nick
authors.initials: N
authors.lastname: Lane
mesh_terms: D000818:Animals; D005075:Biological Evolution; D005260:Female; D005854:Germ Cells; D008928:Mitochondria / Q000235:genetics*; D009865:Oocytes; D012641:Selection, Genetic