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.
Highlights
In distinguishing between the germline and soma, Weismann argued that the division of labour enabled the specialization of cells in somatic tissues, permitting greater organismal complexity [1]
Our analysis reveals that selection for mitochondrial quality can explain many long-puzzling features of germline evolution, including the widespread stability of somatic gametogenesis in plants and basal metazoans, the secondary association between germline sequestration and complexity, the conditions required for early germline sequestration, and other peculiarities of female germline development, including extreme oogamy, follicular atresia, and the putative germline bottleneck
Gametes are formed by meiosis late in development from the same stem cells that give rise to adult somatic cells, which we call somatic gametogenesis (Fig 1a)
Summary
In distinguishing between the germline and soma, Weismann argued that the division of labour enabled the specialization of cells in somatic tissues, permitting greater organismal complexity [1]. The strict distinction between germline and soma stabilises multicellular cooperation, as the only way for somatic cells to increase fitness is by cooperating with their kin in the germline [4,5,6]. According to this theory, plants did not evolve a germline because their rigid cell walls restrict cell movement, limiting the systemic effects of any parasitic cell lines [4]. The range of conditions under which selfish competition could give rise to the germline is seriously restricted, if feasible at all [9]
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