Life-history trait variation in native versus invasive asexual New Zealand mud snails.

Potamopyrgus antipodarum is a New Zealand freshwater snail that is invasive worldwide. While native P. antipodarum populations are characterized by frequent coexistence between obligately sexual and obligately asexual individuals, only the asexual snails are known to invade other ecosystems. Despite low genetic diversity and the absence of sex, invasive asexual P. antipodarum are highly successful. Here, we quantified variation in three key life-history traits across invasive P. antipodarum lineages and compared this variation to already documented variation in these same traits in asexual native lineages to provide a deeper understanding of why some lineages become invasive. In particular, we evaluated if invasive lineages of P. antipodarum could be successful because they represent life-history variation from native ancestors that could facilitate invasion. We found that invasive snails displayed a non-representative sample of native diversity, with invasive snails growing more slowly and maturing more rapidly than their native counterparts. These results are consistent with expectations of a scenario where invasive lineages represent a subset of native variation that is beneficial in the setting of invasion. Together, these results help illuminate the mechanisms driving the worldwide expansion of invasive populations of these snails.

Phosphorus availability in the source population influences response to dietary phosphorus quantity in a New Zealand freshwater snail.

We investigated whether previously documented variation among populations in availability of dietary phosphorus (P) is linked to heterogeneity in growth rate of the New Zealand freshwater snail Potamopyrgus antipodarum on a P-limited diet. We chose this system because P. antipodarum inhabits water bodies that vary in P availability and because P. antipodarum growth rate varies considerably in response to low P. We quantified specific growth rate and alkaline phosphatase (AP) expression in a diverse array of juvenile P. antipodarum fed high vs. low-P diets. We found strong associations between P content of epilithon in the source lake and P. antipodarum growth rate on high vs. low-P diets, with snails collected from lakes with relatively low-P epilithon showing the greatest increase in growth rate on the high-P relative to low-P diet. We also found substantial intraspecific variation in growth response to P limitation. Expression of AP also varied among lineages and was negatively associated with C: P of lake epilithon but did not explain the relationship between C: P in the lake of origin and sensitivity to P limitation. Together, our results demonstrate a strong signature of the P environment in the lake of origin on how this snail responds to P limitation as well as preliminary evidence for intraspecific variation of AP expression in animals.

Discordance between nuclear and mitochondrial genomes in sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum.

The presence and extent of mitonuclear discordance in coexisting sexual and asexual lineages provides insight into 1) how and when asexual lineages emerged, and 2) the spatial and temporal scales at which the ecological and evolutionary processes influencing the evolution of sexual and asexual reproduction occur. Here, we used nuclear single-nucleotide polymorphism (SNP) markers and a mitochondrial gene to characterize phylogeographic structure and the extent of mitonuclear discordance in Potamopyrgus antipodarum. This New Zealand freshwater snail is often used to study the evolution and maintenance of sex because obligately sexual and obligately asexual individuals often coexist. While our data indicate that sexual and asexual P. antipodarum sampled from the same lake population are often genetically similar, suggesting recent origin of these asexuals from sympatric sexual P. antipodarum, we also found significantly more population structure in sexuals vs. asexuals. This latter result suggests that some asexual lineages originated in other lakes and/or in the relatively distant past. When comparing mitochondrial and nuclear population genetic structure, we discovered that one mitochondrial haplotype ('1A') was rare in sexuals, but common and widespread in asexuals. Haplotype 1A frequency and nuclear genetic diversity were not associated, suggesting that the commonness of this haplotype cannot be attributed entirely to genetic drift and pointing instead to a role for selection.

Effects of polyploidy and reproductive mode on life history trait expression.

Ploidy elevation is increasingly recognized as a common and important source of genomic variation. Even so, the consequences and biological significance of polyploidy remain unclear, especially in animals. Here, our goal was to identify potential life history costs and benefits of polyploidy by conducting a large multiyear common garden experiment in Potamopyrgus antipodarum, a New Zealand freshwater snail that is a model system for the study of ploidy variation, sexual reproduction, host-parasite coevolution, and invasion ecology. Sexual diploid and asexual triploid and tetraploid P. antipodarum frequently coexist, allowing for powerful direct comparisons across ploidy levels and reproductive modes. Asexual reproduction and polyploidy are very often associated in animals, allowing us to also use these comparisons to address the maintenance of sex, itself one of the most important unresolved questions in evolutionary biology. Our study revealed that sexual diploid P. antipodarum grow and mature substantially more slowly than their asexual polyploid counterparts. We detected a strong negative correlation between the rate of growth and age at reproductive maturity, suggesting that the relatively early maturation of asexual polyploid P. antipodarum is driven by relatively rapid growth. The absence of evidence for life history differences between triploid and tetraploid asexuals indicates that ploidy elevation is unlikely to underlie the differences in trait values that we detected between sexual and asexual snails. Finally, we found that sexual P. antipodarum did not experience discernable phenotypic variance-related benefits of sex and were more likely to die before achieving reproductive maturity than the asexuals. Taken together, these results suggest that under benign conditions, polyploidy does not impose obvious life history costs in P. antipodarum and that sexual P. antipodarum persist despite substantial life history disadvantages relative to their asexual counterparts.

Distinct Bacterial Microbiomes in Sexual and Asexual Potamopyrgus antipodarum, a New Zealand Freshwater Snail.

Different reproductive strategies and the transition to asexuality can be associated with microbial symbionts. Whether such a link exists within mollusks has never been evaluated. We took the first steps towards addressing this possibility by performing pyrosequencing of bacterial 16S rRNA genes associated with Potamopyrgus antipodarum, a New Zealand freshwater snail. A diverse set of 60 tissue collections from P. antipodarum that were genetically and geographically distinct and either obligately sexual or asexual were included, which allowed us to evaluate whether reproductive mode was associated with a particular bacterial community. 2624 unique operational taxonomic units (OTU, 97% DNA similarity) were detected, which were distributed across ~30 phyla. While alpha diversity metrics varied little among individual samples, significant differences in bacterial community composition and structure were detected between sexual and asexual snails, as well as among snails from different lakes and genetic backgrounds. The mean dissimilarity of the bacterial communities between the sexual and asexual P. antipodarum was 90%, largely driven by the presence of Rickettsiales in sexual snails and Rhodobacter in asexual snails. Our study suggests that there might be a link between reproductive mode and the bacterial microbiome of P. antipodarum, though a causal connection requires additional study.

Response to phosphorus limitation varies among lake populations of the freshwater snail Potamopyrgus antipodarum.

Local adaptation--typically recognized as higher values of fitness-related traits for native vs. non-native individuals when measured in the native environment--is common in natural populations because of pervasive spatial variation in the intensity and type of natural selection. Although local adaptation has been primarily studied in the context of biotic interactions, widespread variation in abiotic characteristics of environments suggests that local adaptation in response to abiotic factors should also be common. Potamopyrgus antipodarum, a freshwater New Zealand snail that is an important model system for invasion biology and the maintenance of sexual reproduction, exhibits local adaptation to parasites and rate of water flow. As an initial step to determining whether P. antipodarum are also locally adapted to phosphorus availability, we examined whether populations differ in their responses to phosphorus limitation. We found that field-collected juvenile P. antipodarum grew at a lower rate and reached an important size threshold more slowly when fed a relatively low vs. a relatively high-phosphorus diet. We also detected significant across-population variation in individual growth rate. A marginally significant population-by-dietary phosphorus interaction along with a two-fold difference across populations in the extent of suppression of growth by low phosphorus suggests that populations of P. antipodarum may differ in their response to phosphorus limitation. Local adaptation may explain this variation, with the implication that snails from lakes with relatively low phosphorus availability should be less severely affected by phosphorus limitation than snails from lakes with higher phosphorus availability.