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.

Intimate Relations—Mitochondria and Ageing

“…Mutation rates of mitochondrial DNA are estimated to be approximately 10–70-fold higher than nuclear DNA [ 11 , 12 ]. This high rate has been attributed to several different causes.…”

Peer Review #1 of "Horizontally transferred genes in the ctenophore Mnemiopsis leidyi (v0.1)"

“…Manuscript to be reviewed there are inconsistencies between studies regarding which animal groups have sequestered germlines (Buss, 1983;Radzvilavicius et al 2016;Jensen et al 2016). The major challenges for HGT detection efforts have been taxon sampling and contamination.…”

Mitochondria—A billion years of cohabitation

“…A recent study in PLOS Biology by Nick Lane and colleagues [1] suggests that the need to pass on high-quality mitochondria to our offspring has determined how organisms choose which cells will contribute to the next generation. Plants can generate gametes from many parts of their bodies, even relatively late in development, producing flowers from recently grown stems.…”

“…A recent study [1] suggests that the choice of strategy is driven by mitochondrial mutation rate. Image credit : journal .…”