Positive and negative frequency-dependent parasitism in naturally co-occurring diploid sexual and polyploid asexual...

Polyploidization is an important evolutionary force. It drives sympatric speciation through reproductive isolation of different cytotypes, and often leads to loss of sexual reproduction in polyploid lineages. Polyploidization and asexuality can change how other species engage in ecological interactions with the polyploid lineage and may change coevolutionary dynamics. Here, we quantified the phenotypic divergence in the freshwater oligochaete worm Lumbriculus variegatus, the California blackworm, among its co-occurring sexual diploid (Lineage II) and asexual polyploid (Lineage I) lineages. We further investigated variation in parasite communities and infection prevalence among sympatric and allopatric diploid/polyploid populations. 10 out of 18 populations showed co-existence of both lineages, with 7 populations harbouring only the polyploid lineage. Both worm lineages hosted endoparasitic nematodes, an ectoparasitic rotifer, and one potentially symbiotic gut ciliate. The parasite community similarity and overlapping size range of diploid and polyploid worms points to the ecological similarity of the worm lineages, despite the substantial ploidy and reproductive strategy differentiation. Although parasite prevalence varied independently of worm lineage, the prevalence was associated with the frequency of local cytotypes. Specifically, the rotifer prevalence was highest on the rare local cytotype, and nematode prevalence was highest on the common local cytotype. These results suggest the presence of both positive and negative frequency-dependent parasitism, which may contribute to the co-existence in the L. variegatus species complex.