Abstract
Genetic diversity is expected to be proportional to population size, yet, there is a well-known, but unexplained lack of genetic diversity in large populations—the “Lewontin’s paradox.” Larger populations are expected to evolve lower mutation rates, which may help to explain this paradox. Here, we test this conjecture by measuring the spontaneous mutation rate in a ubiquitous unicellular marine phytoplankton species Emiliania huxleyi (Haptophyta) that has modest genetic diversity despite an astronomically large population size. Genome sequencing of E. huxleyi mutation accumulation lines revealed 455 mutations, with an unusual GC-biased mutation spectrum. This yielded an estimate of the per site mutation rate µ = 5.55×10−10 (CI 95%: 5.05×10−10 – 6.09×10−10), which corresponds to an effective population size Ne ∼ 2.7×106. Such a modest Ne is surprising for a ubiquitous and abundant species that accounts for up to 10% of global primary productivity in the oceans. Our results indicate that even exceptionally large populations do not evolve mutation rates lower than ∼10−10 per nucleotide per cell division. Consequently, the extreme disparity between modest genetic diversity and astronomically large population size in the plankton species cannot be explained by an unusually low mutation rate.
Highlights
The level of genetic diversity in a population is determined by the balance between the new mutations occurring in the population and the loss of polymorphisms by stochastic processes and selection (Leffler et al 2012; Ellegren and Galtier 2016)
To measure the spontaneous mutation rate in E. huxleyi, we conducted a mutation accumulation (MA) experiment (Halligan and Keightley 2009) that included 15 MA lines grown under standard lab conditions for 232 generations on an average, totaling 3,480 generations across all MA lines
In order to identify the mutations accumulated during the MA experiment, we used Illumina high-throughput sequencing to sequence the genomes of the MA lines at the beginning and the end of MA experiment
Summary
The level of genetic diversity in a population is determined by the balance between the new mutations occurring in the population and the loss of polymorphisms by stochastic processes (drift) and selection (Leffler et al 2012; Ellegren and Galtier 2016). Drift is weaker in larger populations (Crow and Kimura 1970), larger populations are expected to contain more genetic diversity. Selection is expected to be more powerful in populations of larger size, potentially allowing selection to reduce mutation rate to lower values in larger populations (Lynch 2010; Sung, Ackerman, ß The Author(s) 2020.
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