Selection efficacy differs between lifestages in the haploid-diploid Marchantia polymorpha subsp. ruderalis

Ploidy has profound effects on evolution. Perhaps the most compelling effect is related to dominance: In cells with more than one genome copy, the effects of non-dominant deleterious variants are ‘masked’ to some extent, leading to a reduction in the efficacy of selection. This, in turn, leads to increased levels of nucleotide diversity, and it may also affect nucleotide substitution rates.

To test this predicted association between ploidy and the efficacy of selection, we studied genome scale per-gene patterns of genetic diversity and divergence in the genome of the haploid-diploid bryophyte Marchantia. We treated lifestage gene expression bias as a continuous covariate and accounted for genomic autocorrelation patterns using smoothing splines in a general additive regression model (GAM) framework.

Consistent with a lower efficacy of purifying selection, we found increased levels of sequence diversity, Watterson’s θ , and net divergence at non-degenerate sites in genes with diploid-biased gene expression. These genes also showed reduced levels of codon usage bias. In addition, we found chromosome 5 to be an outlier with overall decreased levels of diversity, the site-frequency spectrum skewed towards common alleles, and increased linkage disequilibrium.

In this study, we show the utility of generalized additive models in population genomics, and we present evidence for a ploidy associated difference in the efficacy of selection. We discuss parallels to the evolution of (diploid) sex chromosomes and why the patterns observed are unlikely to be mediated by masking.