Parthenogenetic Panagrolaimus species evolve at lower mutation rates, but show increased nucleotide diversity

Abstract

Asexual reproduction is assumed to lead to the accumulation of deleterious mutations (Muller’s ratchet), and reduced heterozygosity due to the absence of recombination. Panagrolaimid nematodes display different modes of reproduction. Sexual reproduction through distinct males and females, asexual reproduction through parthenogenesis found in the genus Panagrolaimus, and hermaphroditism, found in Propanagrolaimus. Here, we compared genomic features of free-living nematode populations with different reproduction modes isolated from geographically distant regions to study genomic diversity and genome-wide differentiation. We firstly estimated genome-wide spontaneous mutation rates per genome for a polyploid parthenogenetic Panagrolaimus strain and a diploid hermaphroditic Propanagrolaimus species via mutation-accumulation-lines. Secondly, we calculated population genomic parameters including nucleotide diversity and fixation index (F_ST) between populations of asexually and sexually reproducing nematodes. Thirdly, we used phylogenetic network methods on sexually and asexually reproducing Panagrolaimus strains to understand evolutionary relationships between them. The estimated mutation rate was slightly lower for the asexual strain, as expected for taxa with this reproductive mode. Natural polyploid asexual strains revealed higher nucleotide diversity. Despite their common ancestor, a gene network revealed a high level of genetic differentiation among asexual strains. The elevated heterozygosity found in the triploid parthenogens could be explained by the third genome copy. Given their tendentially lower mutation rates it can be hypothesized that this is part of the mechanism to evade Muller’s ratchet. Our findings in parthenogenetic triploid nematode populations seem to challenge common expectations of evolution under asexuality.