DNA Content Variation and SNP Diversity Within a Single Population of Asexual Snails

Abstract

A growing body of research suggests that many clonal populations maintain genetic diversity even without occasional sexual reproduction. The purpose of our study was to document variation in SNP diversity, DNA content, and pathogen susceptibility in clonal lineages of the New Zealand freshwater snail, Potamopyrgus antipodarum. We studied snails that were collected from multiple field sites around a single lake (Lake Alexandrina), as well as isofemale clonal lineages that had been isolated and maintained in the laboratory. We used the KASP method to genotype our samples at 46 nuclear SNP sites, and we used flow cytometry to estimate DNA content. We found high levels of SNP diversity, both in our field samples and in our clonal laboratory lines. We also found evidence of high variation in DNA content among clones, even among clones with identical genotypes across all SNP sites. Controlled pathogen exposures of the laboratory populations revealed variation in susceptibility among distinct clonal genotypes, which was independent of DNA content. Taken together, these results show high levels of diversity among asexual snails, especially for DNA content, and they suggest rapid genome evolution in asexuals.

Asexuality Associated with Marked Genomic Expansion of Tandemly Repeated rRNA and Histone Genes

“…3 B ). These data are consistent with multiple previous lines of evidence pointing to wide intra-ploidy genome size variation in P. antipodarum ( Wallace 1992 ; Neiman et al 2011 ; Paczesniak et al 2013 ; Million et al 2021 ). Indeed, genome-size variation across certain accessions of A. thaliana is largely due to differences in rDNA abundance ( Long et al 2013 ).…”

“…Indeed, genome-size variation across certain accessions of A. thaliana is largely due to differences in rDNA abundance ( Long et al 2013 ). Accordingly, we suggest that the wide range in rDNA–histone genomic content we observed among asexual P. antipodarum may play a key role in observed intraploidy genome size variation in this species ( Neiman et al 2011 ; Million et al 2021 ).…”

“…Unequal crossover during meiotic homologous recombination is a common mechanism for copy number change ( Hastings et al 2009 ) and sequence evolution in rDNA ( Eickbush and Eickbush 2007 ). Although we cannot formally exclude this mechanism, the likelihood that asexual P. antipodarum produce offspring via apomictic parthenogenesis ( Phillips and Lambert 1989 ; Hauser et al 1992 ; Dybdahl and Lively 1995 ; Million et al 2021 ) suggests that a mechanism other than homologous recombination might be involved. One possibility is that rDNA copy number increase in asexual P. antipodarum could arise from unequal sister chromatid exchange (USCE) during apomictic recombination.…”

“…This New Zealand freshwater snail is a textbook model system for the study of sex because natural populations of P. antipodarum are characterized by numerous distinct transitions to obligate asexuality from the ancestral obligate sexual state ( Dybdahl and Lively 1995 ; Paczesniak et al 2013 ) and the frequent coexistence of ecologically and phenotypically similar sexual and asexual individuals ( Lively 1987 ; Jokela et al 1997 ). Nuclear genotyping studies of offspring produced by female P. antipodarum collected from a variety of all- or nearly all-female populations in Europe and New Zealand ( Phillips and Lambert 1989 ; Hauser et al 1992 ) or clonal lineages cultured in the laboratory ( Million et al 2021 ) have invariably indicated reliable preservation of multilocus nuclear genotypes, suggesting strongly that asexual female P. antipodarum are obligately apomictic.…”

Parasitic manipulation or by-product of infection: an experimental approach using trematode-infected snails

“…The snails were collected from 14 different sites around the lake by pushing a kick net through the submerged roots of willow trees. Snails in this shallow region of the lake are predominately diploid sexuals (Vergara et al , 2013), but the region also contains a diverse clonal population {Fox et al, 1996, 98; Million et al, 2021, 2916; Paczesniak et al, 2014, 2219}, which shows rapid turnover in clone frequencies, most likely driven by parasite-mediated frequency-dependent selection {Paczesniak, 2014, 2219}. The frequency of infection also oscillates over time such that the sexual diploids are more or less infected than the polyploid asexuals (Gibson et al , 2018).…”