Male offspring production by asexual Potamopyrgus antipodarum, a New Zealand snail

As only females contribute directly to population growth, sexual females investing equally in sons and daughters experience a two-fold cost relative to asexuals producing only daughters. Typically, researchers have focused on benefits of sex that can counter this 'cost of males' and thus explain its predominance. Here, we instead ask whether asexuals might also pay a cost of males by quantifying the rate of son production in 45 experimental populations ('lineages') founded by obligately asexual female Potamopyrgus antipodarum. This New Zealand snail is a powerful model for studying sex because phenotypically similar sexual and asexual forms often coexist, allowing direct comparisons between sexuals and asexuals. After 2 years of culture, 23 of the 45 lineages had produced males, demonstrating that asexual P. antipodarum can make sons. We used maximum-likelihood analysis of a model of male production in which only some lineages can produce males to estimate that ~50% of lineages have the ability to produce males and that ~5% of the offspring of male-producing lineages are male. Lineages producing males in the first year of the experiment were more likely to make males in the second, suggesting that some asexual lineages might pay a cost of males relative to other asexual lineages. Finally, we used a simple deterministic model of population dynamics to evaluate how male production affects the rate of invasion of an asexual lineage into a sexual population, and found that the estimated rate of male production by asexual P. antipodarum is too low to influence invasion dynamics.     

Multiple paternity in the freshwater snail,Potamopyrgus antipodarum

Mating multiply may incur costs, such as exposure to predators and to sexually transmitted diseases. Nevertheless, it may be favored, in spite of these costs, as a way to increase the genetic diversity of offspring through fertilization by multiple males. Here, we tested for multiple paternity in a freshwater snail (Potamopyrgus antipodarum), which is host to several species of sterilizing trematode worms. Using microsatellites markers, we found multiple paternity in two different snail populations, with as many as seven males fertilizing a single female. In addition, high evenness of sire fertilization was found within individual broods. Multiple paternity can occur for a variety of reasons; however, given that these populations experience high risk of infection by a sterilizing trematode, one potential explanation may be that multiple paternity and high evenness of sire fertilizations increase the chances of the production of parasite‐resistant offspring.     

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.     

Variation in asexual lineage age in Potamopyrgus antipodarum, a New Zealand snail

Asexual lineages are thought to be subject to rapid extinction because they cannot generate recombinant offspring. Accordingly, extant asexual lineages are expected to be of recent derivation from sexual individuals. We examined this prediction by using mitochondrial DNA sequence data to estimate asexual lineage age in populations of a freshwater snail (Potamopyrgus antipodarum) native to New Zealand and characterized by varying frequency of sexual and asexual individuals. We found considerable variation in the amount of genetic divergence of asexual lineages from sexual relatives, pointing to a wide range of asexual lineage ages. Most asexual lineages had close genetic ties (approximately 0.1% sequence divergence) to haplotypes found in sexual representatives, indicating a recent origin from sexual progenitors. There were, however, two asexual clades that were quite genetically distinct (> 1.2% sequence divergence) from sexual lineages and may have diverged from sexual progenitors more than 500,000 years ago. These two clades were found in lakes that had a significantly lower frequency of sexual individuals than lakes without the old clades, suggesting that the conditions that favor sex might select against ancient asexuality. Our results also emphasize the need for large sample sizes and spatially representative sampling when hypotheses for the age of asexual lineages are tested to adequately deal with potential biases in age estimates.     

Diverse,endemic and polyphyletic clones in mixed populations of a freshwater snail (Potamopyrgus antipodarum)

Understanding the source and diversity of clones is necessary to resolve the complicated issues surrounding the apparent evolutionary stability of sexual reproduction. The source of clones is important because present theory is based on an “all else equal” assumption, which is predicated on the idea that clonal mutants are derived from and compete with local sexual populations. Clonal diversity is important because it reduces the advantage of sexual reproduction under either soft selection (the Tangled Bank Hypothesis) or under strict frequency-dependent selection (the Red Queen Hypothesis). In the present study, protein electrophoresis was used to determine the source and diversity of clones in a freshwater snail (Potamopyrgus antipodarum) in four glacial lakes in which sexual and clonal females were thought to coexist. The results showed (1) that the populations were mixtures of diploid sexual and triploid asexual individuals, (2) that genotypic diversity of clonal populations is very high in all four lakes (but lower than in the sympatric sexual populations), and (3) that the clones are polyphyletically derived from their sympatric sexual populations. Consequently, repeated mutation to parthenogenetic reproduction since the Pleistocene has introduced a different and diverse set of clones in all four lakes. Such diversity may provide a challenge for the ecological theories of sex that rely on frequency-dependent selection.     

Embryo production in a parthenogenetic snail (Potamopyrgus antipodarum) is negatively affected by the presence of other parthenogenetic females

Abstract. Stimuli associated with copulatory behavior are often needed to maximize reproductive output in internally fertilized sexual taxa. Although non-pseudogamous parthenogenetic females have no need for sperm, parthenogens descended from sexual ancestors may still require copulatory stimuli to reach their full reproductive potential. Retention of physiological dependence on copulation in parthenogens could facilitate the maintenance of sexual reproduction in species where sexual and parthenogenetic individuals coexist if parthenogens do not receive enough copulatory stimuli to achieve maximal daughter production. A laboratory experiment was conducted to determine whether embryo production in parthenogenetic female snails ( Potamopyrgus antipodarum ) is dependent on male presence. Rather than male presence, this experiment showed that embryo production is affected by the number of coexisting parthenogens. Specifically, parthenogens housed with fewer other parthenogens produced significantly more embryos than parthenogens housed with a greater number of other parthenogens, regardless of male presence and total population size. This result indicates that copulatory dependence is not likely to contribute to the maintenance of sex in P. antipodarum . Instead, it demonstrates that females of P. antipodarum negatively affect each other's reproduction, and suggests that females of P. antipodarum may exert a larger competitive influence than males of P. antipodarum . Moreover, this finding raises the possibility that highly parthenogenetic and consequently female-dense populations of P. antipodarum may experience decreased reproductive output when population size is large and resources are limiting.     

Pleistocene glaciation is implicated in the phylogeographical structure of Potamopyrgus antipodarum, a New Zealand snail

Pleistocene glaciation has been identified as an important factor shaping present-day patterns of phylogeographical structure in a diverse array of taxa. The purpose of this study was to use mitochondrial sequence data to address whether Pleistocene glaciation is also a major determinant of phylogeographical patterns in Potamopyrgus antipodarum, a freshwater snail native to New Zealand. We found that haplotypes were separated by no more than 3.7% sequence divergence, and major genetic divisions tended to occur on a north-south axis. These data fit the predictions of the hypothesis that isolation of P. antipodarum in glacial refugia at the northern and southern tip of the South Island of New Zealand during the Pleistocene glaciation underlies the present-day phylogeographical structure. Because sexual P. antipodarum occasionally produce asexual offspring, we also used these data to show that the appearance of asexuality is not phylogeographically constrained. This means that the maintenance of sex in P. antipodarum cannot be wholly due to limited contact between sexual and asexual lineages and must instead be linked to a selective advantage of sexual reproduction.     

Effect of starvation on parasite-induced mortality in a freshwater snail (Potamopyrgus antipodarum)

The level of host exploitation is expected, under theory, to be selected to maximise (subject to constraints) the lifetime reproductive success of the parasite. Here we studied the effect of two castrating trematode species on their intermediate snail host, Potamopyrgus antipodarum. One of the trematode species, Microphallus sp., encysts in the snail host and the encysted larvae “hatch” following ingestion of infected snails by birds. The other species, Notocotylus gippyensis, by contrast, releases swimming larvae; ingestion of the snail host is not required for, and does not aid, transmission to the final host. We isolated field-collected snails for 3 months in the laboratory, and followed the survival of infected and uninfected snails under two conditions: not fed and fed ad libitum. Mortality of the infected hosts was higher than mortality of the uninfected ones, but the response to starvation treatment was parasite species specific. N. gippyensis induced significantly higher mortality in starved snails than did Microphallus. Based on these results, we suggest that host exploitation by different species of trematodes may depend on the type of transmission. Encysting in the snail host may select for a reduced rate of host exploitation so as to increase the probability of transmission to the final host. Received: 29 July 1998 / Accepted: 1 February 1999     

Wide variation in ploidy level and genome size in a New Zealand freshwater snail with coexisting sexual and asexual lineages

Natural animal populations are rarely screened for ploidy-level variation at a scale that allows detection of potentially important aberrations of common ploidy patterns. This type of screening can be especially important for the many mixed sexual/asexual systems in which sexuals are presumed to be dioecious diploids and asexuals are assumed to be triploid and all-female. For example, elevation of ploidy level above triploidy can be a source of genetic variation and raises the possibility of gene flow among ploidy levels and to asexual lineages. We used flow cytometry and mtDNA sequencing to characterize ploidy level and genome size in Potamopyrgus antipodarum, a New Zealand freshwater snail where obligate sexual (presumed diploid and dioecious) and obligate apomictic asexual (presumed triploid and nearly all female) individuals frequently coexist. We documented the widespread occurrence and multiple origins of polyploid males and individuals with >3× ploidy, and find that both are likely to be descended from asexual females. Our survey also suggested the existence of extensive variation in genome size. The discovery of widespread variation in ploidy level and genome size in such a well-studied system highlights the importance of broad, extensive, and ecologically representative sampling in uncovering ploidy level and genome-size variation in natural populations.     

Invasion of the New Zealand mud snail (Potamopyrgus antipodarum) in the Green River below Flaming Gorge Dam

Biological Invasions - New Zealand mud snails (Potamopyrgus antipodarum) were first introduced to the United States in 1987 and have subsequently invaded water bodies across the United States. At...     

Isolation and characterization of di‐ and trinucleotide microsatellites in the freshwater snail Potamopyrgus antipodarum

The freshwater prosobranch snail Potamopyrgus antipodarum is an important model system for studying the maintenance of sexual reproduction in its native New Zealand. Since introduction to the UK in the 1850s, the species has spread throughout Europe and recently the USA. We present the first microsatellites for P. antipodarum. Using two isolation protocols, which are qualitatively compared, we have developed PCR primers for three di‐ and four trinucleotide microsatellites. All loci proved to be polymorphic, when screened for variability in several UK populations. These markers should be of considerable utility in future population and ecological genetics studies of this species.     

Parasite resistance predicts fitness better than fecundity in a natural population of the freshwater snail Potamopyrgus antipodarum

The cost of males should give asexual females an advantage when in competition with sexual females. In addition, high‐fecundity asexual genotypes should have an advantage over low‐fecundity clones, leading to reduction in clonal diversity over time. To evaluate fitness components in a natural population, we measured the annual reproductive rate of individual sexual and asexual female Potamopyrgus antipodarum, a New Zealand freshwater snail, in field enclosures that excluded competitors and predators. We used allozyme genotyping to assign the asexual females to particular clonal genotypes. We found that the most fecund asexual clones had similar or higher fecundity as the top 10% of sexual families, suggesting that fecundity selection, even without the cost of males, would lead to replacement of the sexual population by clones. Consequently, we expected that the clones with the highest fecundity would dominate the natural population. Counter to this prediction, we found that high annual reproductive rates did not correlate with the frequency of clones in the natural population. When we exposed the same clones to parasites in the laboratory, we found that resistance to infection was positively correlated with the frequency of clones in the population. The correlation between fecundity and parasite resistance was negative, suggesting a trade‐off between these two traits. Our results thus suggest that parasite resistance is an important short‐term predictor of the success of asexual P. antipodarum in this population.     

Clonal structure of the introduced freshwater snail Potamopyrgus antipodarum (Prosobranchia: Hydrobiidae), as revealed by DNA fingerprinting.

Multi-locus DNA fingerprints were obtained from individuals of the hydrobiid snail, Potamopyrgus antipodarum (= P. jenkinsi), by using an RNA derivative (pSPT 18.15) of Jeffrey's 33.15 minisatellite core sequence. Whole-body homogenization of snails yielded 3.21 +/- 0.09 micrograms DNA per individual, producing complex profiles comprising 12-22 fragments within the 1.0-20.0 kilobase (kb) size range. Fingerprints from natural and experimental populations identified three distinct clonal genotypes corresponding to morphological strains A, B and C, with only rare mutational variants. Mother-offspring comparisons of genetic fingerprints revealed genetic stability during apomictic parthenogenesis. Data support the notion that British populations of P. antipodarum comprise three widespread obligate parthenogenetic clones resulting from a mid-19th Century introduction from Australasia. The present-day low levels of genotypic diversity are discussed in relation to the typical occurrence of P. antipodarum in man-made or immature habitats.     

Stay in shape: Assessing the adaptive potential of shell morphology and its sensitivity to temperature in the invasive New Zealand mud snail Potamopyrgus antipodarum through phenotypic plasticity and natural selection in Europe

Climate change may force organisms to adapt genetically or plastically to new environmental conditions. Invasive species show remarkable potential for rapid adaptation. The ovoviviparous New Zealand mud snail (NZMS), Potamopyrgus antipodarum, has successfully established across Europe with two clonally reproducing mitochondrial lineages since its arrival in the first half of the 19th century. Its remarkable variation in shell morphology was shown to be fitness relevant. We investigated the effects of temperature on shell morphology across 11 populations from Germany and the Iberian Peninsula in a common garden across three temperatures. We analyzed size and shape using geometric morphometrics. For both, we compared reaction norms and estimated heritabilities. For size, the interaction of temperature and haplotype explained about 50% of the total variance. We also observed more genotype by environment interactions indicating a higher degree of population differentiation than in shape. Across the three temperatures, size followed the expectations of the temperature‐size rule, with individuals growing larger in cold environments. Changes in shape may have compensated for changes in size affecting space for brooding embryos. Heritability estimates were relatively high. As indicated by the very low coefficients of variation for clonal repeatability (CV _A ), they can probably not be compared in absolute terms. However, they showed some sensitivity to temperature, in haplotype t more so than in z, which was only found in Portugal. The low CV _A values indicate that genetic variation among European populations is still restricted with a low potential to react to selection. A considerable fraction of the genetic variation was due to differences between the clonal lineages. The NZMS has apparently not been long enough in Europe to accumulate significant genetic variation relevant for morphological adaptation. As temperature is obviously not the sole factor influencing shell morphology, their interaction will probably not be a factor limiting population persistence under a warming climate in Europe.     

Habitat-specific variation in life-history traits,clonal population structure and parasitism in a freshwater snail (Potamopyrgus antipodarum)

High risk of infection by parasites may select for early reproduction in natural host populations. In a previous study of a freshwater snail (Potamopyrgus antipodarum) we found (1) that different clones of the snail are associated with different depth-structured vegetation zones and (2) that snails in shallow water, where the age-specific risk of infection is highest, mature at a smaller size than snails in deeper habitats. This result suggests that there has been selection for early reproduction in these snails, and that different clonal genotypes have different life-history strategies. Alternatively, the observed life-history variation in the snails might be due to ecological factors that are independent of parasites, but correlated with depth. In the present study, we decoupled parasitism and depth by examining life histories and clonal population structure in a second lake (Lake Tennyson) where the mean prevalence of trematode parasites was low and unrelated to depth. Consistent with the previous results, clones were structured according to vegetation zones in Lake Tennyson. However, we found no relationship between depth and life-history traits, which is inconsistent with the idea that depth-associated factors other than parasites affect snail life histories. Taken together, these results suggest that life-history variation is more likely to result from a depth-specific risk of infection than from depth per se, and that partitioning of habitat zones by different groups of clones may be a general phenomenon in P. antipodarum populations.     

Phosphorus-mediated changes in life history traits of the invasive New Zealand mudsnail (Potamopyrgus antipodarum)

The longer soil has to stay moist to allow germination the more likely that seedlings experience favourable moisture conditions. Since theory predicts that fitness variance-reducing traits will be negatively correlated, we tested the hypothesis that time to germination is negatively correlated with the ability of radicle growth to keep up with the drying front. We measured time to germination and root elongation rate (RER) in 14 Kalahari annuals. We controlled for habitat (canopy association and sand content), germinability, median base water potential for germination (ψ ₅₀), seed mass and seed shape as a persistence surrogate. For species and phylogenetically independent contrasts (PICs), we did not find a relationship between time to germination and RER. However, we found a negative relationship of time to germination with RER for PICs when controlling for sand content and ψ ₅₀. Seed shape increased with time to germination which can be explained by reduced opportunities for germination in slow-germinating species that select for persistence. We found a positive relationship between time to germination and ψ ₅₀, suggesting a continuum of risky to cautious germination. ψ ₅₀ was not correlated with RER suggesting that variation in ψ ₅₀ reflects different drought-adapted traits. Probably the relationship of time to germination with RER is not mediated by seed mass, which was not correlated with time to germination as found by others, though RER was positively correlated with seed mass. Instead of the seed size-seed number trade-off, a trade-off with resource capture may explain variation in RER: more root hairs or rootlets may increase resource capturing surface while reducing RER. For habitat, we found a (positive) relationship with time to germination only for canopy association. This may be explained by maximization of resource capture at the expense of RER being favoured by the higher nutrient and water availability under canopies. Future studies should clarify which trade-offs govern variation in time to germination, focussing on a possible resource capture-RER trade-off.     

Coexistence in the intertidal: interactions between the non‐indigenous New Zealand mud snail Potamopyrgus antipodarum and the native estuarine isopod Gnorimosphaeroma insulare

Nonindigenous species (NIS) that achieve high densities in their recipient communities are expected to have negative effects on native competitors. However, recent reviews have shown that competitors, unlike predators and parasites, have rarely been documented to cause extinctions. There is a need for better understanding of competitive interactions between nonindigenous species and native competitors across systems where NIS reach high densities. In this paper we examine competitive interactions between the exotic, invasive New Zealand mud snail Potamopyrgus antipodarum and native estuarine invertebrates. P. antipodarum is often described as a freshwater snail but can occur in brackish water as well; it has been established in the Columbia River Estuary for over ten years. We addressed competition in this estuarine system using three approaches: field surveys of the benthic invertebrate community, stable isotope analysis of overlap in resource use by common invertebrates, and a laboratory competition experiment that tested the strength of competition between P. antipodarum and the isopod, Gnorimosphaeroma insulare, which overlap in resource use. We found no evidence of negative competitive impacts of P. antipodarum on native benthic invertebrates in this estuarine system. Densities of P. antipodarum and common native epibenthic invertebrates are positively correlated in the intertidal, likely due to shared habitat preferences. The competition experiment showed that the effect of interspecific competition from P. antipodarum on the foraging and survival of G. insulare was significantly less than the effect of intraspecific competition between isopods. The presence of the isopod G. insulare reduced foraging in P. antipodarum, but this change did not result in reduced survival and growth of snails. Hence, interspecific competition is weak despite high densities achieved by the invading species. Finally, we discuss several possible explanations for the observation that P. antipodarum does not have an obvious negative competitive impact on native benthic invertebrates.