Evolution of Mutation Rate in Astronomically Large Phytoplankton Populations

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.

Keywords: Emiliania huxleyi; Lewontin’s paradox; codon bias; effective population size; mutation accumulation; mutation rate; phytoplankton evolution.

Fig. 1.

Nuclear mutation rate per MA line. Average number of mutations per MA line is ∼30.33 (SD = 11.84). The number of mutations per MA line differs from the theoretical distribution assuming equal mutation rate across the lines (Pearson’s χ² test, χ² = 37.733, P value = 0.0006).

Fig. 2.

Mutation spectrum of Emiliania huxleyi. Transitions occur more frequently than transversions, with observed transition/transversion ratio k = 1.11.

Fig. 3.

Effective population sizes (N_e) and per site mutation rates (µ) in Emiliania huxleyi (star) and other species (blue, animals; dark green, plants; light green, unicellular eukaryotes; red, bacteria) There is a strong negative correlation between N_e and µ (Pearson corr. test, ρ = −0.78 and P value = 5.706×10⁻⁷). Data used for this plot are listed in supplementary table S5, Supplementary Material online.