doi: 10.1371/journal.pbio.2000410. eCollection 2016 Dec.
Selection for Mitochondrial Quality Drives Evolution of the Germline
Affiliations
- PMID:27997535
- PMCID: PMC5172535
- DOI: 10.1371/journal.pbio.2000410
Item in Clipboard
Selection for Mitochondrial Quality Drives Evolution of the Germline
Arunas L Radzvilavicius et al. PLoS Biol..
Display options
Format
Display options
Format
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.
Conflict of interest statement
The authors have declared that no competing interests exist.
Figures
(a) Development from zygote (left-hand side) to adult, showing early tissue differentiation (cells with differing shades) and late formation of gametes (G) from somatic cells in the adult (somatic gametogenesis).(b) Equivalent multicellular development depicting sequestration of gametes early in development (early germline). Dotted line indicates further development; adult and gamete cells not drawn to scale.(c) Copying errors (μS) during replication of mitochondrial DNA.(d) Mutations caused by background damage (μB) from, e.g., ultraviolet (UV) radiation or reactive oxygen species (ROS).(e) Doubling followed by random segregation of mitochondrial mutants (red) at cell division increases variance between daughter cells.(f) Concave fitness function, in which cell fitness declines non-linearly with the accumulation of mitochondrial mutations (μS +μB) as seen in mitochondrial diseases (see text).
At each cell division, the variance in mitochondrial mutant load (m/M) between daughter cells (red plots) increases due to mutational input as well as random segregation, generating cells with both more (above dotted line) and fewer (below dotted line) mutations than the zygotic cell. The blue plots show the variance in mutant load at each division due to mutation alone, without any random segregation.(a) The mutant load increases slowly with each cell division (green line) when the rate of copying errors is low (μS = 0.01).(b) Increasing mitochondrial number (M) decreases the variance in mutant load per cell (red plots) as the effects of random segregational drift are dampened.(c) Increasing copying errors (μS = 0.05) increases the mutant load in daughter cells; segregation no longer generates many high-quality daughter cells with fewer mutations than the zygote. Data were derived from a starting number of mutants in zygotesm = 0.24M, and then run iteratively through successive cell divisions as described in the first section of the Methods. Underlying data can be found at:https://github.com/ArunasRadzvilavicius/GermlineEvolution/tree/master/FigureData .
(a) Heat map showing fixation probability of an allele encoding early germline sequestration (at generationNG = 3) in a simple organism that lacks tissue differentiation and produces gametes by somatic gametogenesis (at generationNG = 10), in relation to the rate of copying errors (μS) and background damage (μB). The early germline mutation is introduced at a frequency of 0.05 (see Methods). Early germline sequestration is favoured by higherμS and lowerμB (blue, top left). The early germline allele is selected against in organisms with lowμS and highμB (red, bottom right), conditions that instead favour somatic gametogenesis. The solid line represents neutrality.(b) Increasing the number of tissues to eight makes it harder to fix an early germline (NG = 3)—the region shaded in red expands (solid line versus dotted line) so germline fixation now requires higherμS and lowerμB compared with (a).(c) Increasing the number of mitochondria to 200 in an organism with eight tissues has little effect on early germline sequestration. Thus, increasing the level of complexity (more tissues and mitochondria) does not favour early germline sequestration. Underlying data can be found at:https://github.com/ArunasRadzvilavicius/GermlineEvolution/tree/master/FigureData .
Adult fitness is a function of zygote fitness (the mutation load inherited), mutational input, and random segregation during development.(a) In organisms with no tissue differentiation, adult fitness is similar to zygote fitness, as the number of new mutations accumulating within a single generation is limited, and variance in mutant load between cells within a tissue has no effect on adult fitness.(b) In organisms with early differentiation of multiple tissues, adult fitness is undermined by segregational variance, as some tissue-precursor cells receive a higher mutant load than others, and adult fitness depends on the function of the worst tissue.(c) Increasing the number of mitochondria decreases the variance in mutant load between tissue-precursor cells, and so reduces the loss in adult fitness caused by random segregation. Parameter valuesμS = 0.01,μB = 0.005, ten cell divisions to adulthood, and a lifespan equivalent to 40 cell division cycles. Underlying data can be found at:https://github.com/ArunasRadzvilavicius/GermlineEvolution/tree/master/FigureData .
(a) The mitochondria in the zygote are partitioned into daughter cells at each cell division. With isogamy (Q = 0, blue), the zygote contains the same numberM mitochondria as normal somatic cells. In contrast, with oogamy (Q = 4, red) the larger number of mitochondria contained in the zygotes (2QM = 800) are partitioned without further replication (over four rounds of cell division) until the standard mitochondrial number (M = 50) is restored.(b) A large oocyte (Q = 4, red) suppresses the variance in mutation load (m/M) in the first few rounds of cell division (left inset) compared with a small oocyte (Q = 0, blue). This early difference in variance is virtually lost after 20 rounds of cell division (right inset). Segregation is modelled as described in the Methods without further accumulation of mutations.M = 50 and for illustrative purposes the mutation frequency set atm = 25.(c) The early reduction in variance produced by oogamy improves adult fitness in organisms with multiple tissues but has practically no effect when there is no tissue differentiation. Mutation rates are set toμS = 0.01 andμB = 0.005, and the number of mitochondria toM = 50. The initial mutant load in the zygote is set to 20% (i.e., 2QM/5).(d) The fixation probability (95% confidence intervals) of an alleleA specifying oogamyQ depends on the number of somatic tissues. IncreasingQ reduces variance in mutant load between tissues, improving somatic fitness (c), but decreases variance among gametes, reducing the efficacy of purifying selection. Moderate levels of mitochondrial oogamy are therefore expected to evolve more readily in organisms with high levels of somatic differentiation. Mutation rates are set toμS = 0.01 andμB = 0.005, and the number of mitochondria toM = 50. The dashed line indicates the fixation probability of a neutral mutant. Underlying data can be found at:https://github.com/ArunasRadzvilavicius/GermlineEvolution/tree/master/FigureData .
(a) Fixation probability (95% confidence intervals) of the alleleg, specifying sequestration of an early germline atNG = 3 cell divisions, decreases with increasing mitochondrial oogamy, especially in organisms with multiple somatic tissues.(b) The early germline atNG = 3 is more likely to fix in organisms with multiple tissues if there are additional germline cell divisions that restore segregational variance between gametes. Parameter valuesμS = 0.01,μB = 0.005,M = 50. The dashed lines indicate the fixation probability of a neutral mutant. Underlying data can be found at:https://github.com/ArunasRadzvilavicius/GermlineEvolution/tree/master/FigureData .
References
- Weismann A. Prof. Weismann’s theory of heredity. Nature. 1890; 41: 317–323.
- Seipel K, Yanze N, Schmid V. The germ line and somatic stem cell gene Cniwi in the jellyfishPodocoryne carnea. Int J Dev Biol. 2004; 48: 1–7. - PubMed
- Buss LW. The Evolution of Individuality. Princeton, New Jersey: Princeton University Press; 1987.
- Michod RE. Cooperation and conflict in the evolution of individuality. II: Conflict mediation. Proc R Soc Lond B. 1996; 263: 813–822. - PubMed
MeSH terms
LinkOut - more resources
Full Text Sources
Other Literature Sources