Adaptive phenotypic plasticity in a clonal invader

Organisms featuring wide trait variability and occurring in a wide range of habitats, such as the ovoviviparous New Zealand freshwater snail Potamopyrgus antipodarum, are ideal models to study adaptation. Since the mid‐19th century, P. antipodarum, characterized by extremely variable shell morphology, has successfully invaded aquatic areas on four continents. Because these obligately and wholly asexual invasive populations harbor low genetic diversity compared to mixed sexual/asexual populations in the native range, we hypothesized that (1) this phenotypic variation in the invasive range might be adaptive with respect to colonization of novel habitats, and (2) that at least some of the variation might be caused by phenotypic plasticity. We surveyed 425 snails from 21 localities across northwest Europe to attempt to disentangle genetic and environmental effects on shell morphology. We analyzed brood size as proxy for fitness and shell geometric morphometrics, while controlling for genetic background. Our survey revealed 10 SNP genotypes nested into two mtDNA haplotypes and indicated that mainly lineage drove variation in shell shape but not size. Physicochemical parameters affected both shell shape and size and the interaction of these traits with brood size. In particular, stronger stream flow rates were associated with larger shells. Our measurements of brood size suggested that relatively larger slender snails with relatively large apertures were better adapted to strong flow than counterparts with broader shells and relatively small apertures. In conclusion, the apparent potential to modify shell morphology plays likely a key role in the invasive success of P. antipodarum; the two main components of shell morphology, namely shape and size, being differentially controlled, the former mainly genetically and the latter predominantly by phenotypic plasticity.     

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.     

Adaptive responses and invasion: the role of plasticity and evolution in snail shell morphology

Invasive species often exhibit either evolved or plastic adaptations in response to spatially varying environmental conditions. We investigated whether evolved or plastic adaptation was driving variation in shell morphology among invasive populations of the New Zealand mud snail (Potamopyrgus antipodarum) in the western United States. We found that invasive populations exhibit considerable shell shape variation and inhabit a variety of flow velocity habitats. We investigated the importance of evolution and plasticity by examining variation in shell morphological traits 1) between the parental and F₁ generations for each population and 2) among populations of the first lab generation (F₁) in a common garden, full‐sib design using Canonical Variate Analyses (CVA). We compared the F₁ generation to the parental lineages and found significant differences in overall shell shape indicating a plastic response. However, when examining differences among the F₁ populations, we found that they maintained among‐population shell shape differences, indicating a genetic response. The F₁ generation exhibited a smaller shell morph more suited to the low‐flow common garden environment within a single generation. Our results suggest that phenotypic plasticity in conjunction with evolution may be driving variation in shell morphology of this widespread invasive snail.     

Genomic evidence for population‐specific responses to co‐evolving parasites in a New Zealand freshwater snail

Reciprocal co‐evolving interactions between hosts and parasites are a primary source of strong selection that can promote rapid and often population‐ or genotype‐specific evolutionary change. These host–parasite interactions are also a major source of disease. Despite their importance, very little is known about the genomic basis of co‐evolving host–parasite interactions in natural populations, especially in animals. Here, we use gene expression and sequence evolution approaches to take critical steps towards characterizing the genomic basis of interactions between the freshwater snail Potamopyrgus antipodarum and its co‐evolving sterilizing trematode parasite, Microphallus sp., a textbook example of natural coevolution. We found that Microphallus‐infected P. antipodarum exhibit systematic downregulation of genes relative to uninfected P. antipodarum. The specific genes involved in parasite response differ markedly across lakes, consistent with a scenario where population‐level co‐evolution is leading to population‐specific host–parasite interactions and evolutionary trajectories. We also used an F_ST‐based approach to identify a set of loci that represent promising candidates for targets of parasite‐mediated selection across lakes as well as within each lake population. These results constitute the first genomic evidence for population‐specific responses to co‐evolving infection in the P. antipodarum‐Microphallus interaction and provide new insights into the genomic basis of co‐evolutionary interactions in nature.     

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.     

Parallel variation among populations in the shell morphology between sympatric native and invasive aquatic snails

A phenotypic response, either plastic or evolved, is often required for successful invasion of novel environments. Populations of the invasive snail Potamopyrgus antipodarum have colonized a wide range of environments in the western U. S. since 1985, but the extent of plastic adjustment and evolved adaptation to local environments is largely unknown. We examined variation in shell morphology among four sites in the Snake River, Idaho, including both still-water and free-flowing river habitats and compared the variation to that of a native snail (Pyrgulopsis robusta) using geometric morphometric techniques. Using Generalized Procrustes analysis, we tested for phenotypic responses by determining (1) whether Po. antipodarum from the four locations differed in shell morphology, and (2) whether these snails exhibited corresponding shell shape variation with sympatric populations of a native snail. Both native and invasive snails exhibited similar variation in shell morphology across three of the four sites. The Canonical Variate assignment test grouped 85 % of both snail species to their rightful sample site. In addition, the Principal Component Analysis displayed similar patterns of shell variation across the four sites, indicating parallel variation in shell shape. For three of the four sites, both the native and invasive snails exhibited differences in shell shape consistent with water flow variation (still-water versus fast free-flowing river). Taken together, these results suggest that the shell shape of the invasive snail has changed either through plasticity or evolution, and that both native and invasive snail populations responded to local environmental conditions in a similar manner.     

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.     

Long-term population fluctuations of the exotic New Zealand mudsnail <Emphasis Type="Italic">Potamopyrgus antipodarum</Emphasis> and its introduced aporocotylid trematode in northwestern France

Long-term studies of invasive populations are rare, which is unfortunate because important aspects of their dynamics may only be detected over long term. For instance, invasive populations can experience substantial population declines, or even crashes, sometime after their introduction and invasion. Potamopyrgus antipodarum (Caenogastropoda) is a successful invader, and is rarely parasitized in introduced areas. In France, the snail is parasitized as first intermediate host by only one trematode species (Aporocotylid sp. I), native to the snail’s home range, New Zealand. Here, we examined the dynamics of the molluscan assemblage in a French stream on a 14-year interval (2000–2004 and 2009–2013), focusing on this introduced host-parasite association. Overall, P. antipodarum was numerically dominant (90.80%) among molluscs, also including sphaeriid clams (9.12%) and pulmonate snails (0.08%). However, during the last monitoring period, we found a substantial population decline of P. antipodarum, potentially driven by environmental change, such as decreased water temperature and depth, and possibly competitive interactions with sphaeriids, which became numerically dominant (56.34%). P. antipodarum was the only mollusc found infected and only by Aporocotylid sp. I. Interestingly, despite low monthly prevalence (from 0 to 1.52%) and snail host population decline, the P. antipodarum-aporocotylid relationship appeared to be persistent over time.     

Ecomorphology of a generalist freshwater gastropod: complex relations of shell morphology,habitat, and fecundity

Evolutionary and ecological situations in a species’ native and invasive ranges can be drastically different. This is the case for Potamopyrgus antipodarum Gray (1843) a morphologically highly variable freshwater snail native to New Zealand, where sexual and asexual individuals coexist and experience selective pressure by sterilizing endoparasites. By contrast, only a few asexual lineages have been established in invaded regions around the globe, where parasite infection is extremely rare. We analyzed the ecomorphology of 996 native P. antipodarum in a geometric morphometric framework, using brood size as proxy for fecundity, and mtDNA and nuclear SNPs to account for relatedness and identify reproductive mode. As expected, we found genetic and morphological diversity to be higher in native than in invasive snails investigated previously, but surprisingly no higher morphological diversity in sexual versus asexual individuals. The relationships between shell morphology, habitat, and fecundity were complex. Shape variation was primarily linked to genetic relatedness but specific environmental factors including flow rate induced similar shell shapes. By contrast, shell size was largely explained by environmental factors. Fecundity was correlated with size but showed trade-offs with shape in increasingly extreme conditions. With increasing flow and toward small springs, the trend of shell shape becoming wider was reversed, i.e., snails with narrower shells were brooding more embryos. We concluded that both genetic and environmental contributions to variation in shell morphology in P. antipodarum likely play an important role in the ability of this species to adapt to a wide spectrum of habitats.     

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.     

Changes in the selection differential exerted on a marine snail during the ontogeny of a predatory shore crab

Empirical estimates of selection gradients caused by predators are common, yet no one has quantified how these estimates vary with predator ontogeny. We used logistic regression to investigate how selection on gastropod shell thickness changed with predator size. Only small and medium purple shore crabs (Hemigrapsus nudus) exerted a linear selection gradient for increased shell‐thickness within a single population of the intertidal snail (Littorina subrotundata). The shape of the fitness function for shell thickness was confirmed to be linear for small and medium crabs but was humped for large male crabs, suggesting no directional selection. A second experiment using two prey species to amplify shell thickness differences established that the selection differential on adult snails decreased linearly as crab size increased. We observed differences in size distribution and sex ratios among three natural shore crab populations that may cause spatial and temporal variation in predator‐mediated selection on local snail populations.     

The effects of dredging and fish stocking on the trophic status of shallow,peaty ditches

Size selective predation on molluscs was apparent for lake trout (Salvelinus namaycush) and round whitefish (Prosopium cylindraceum), but not for arctic grayling (Thymallus arcticus), in the Toolik Lake region of arctic Alaska during the summer of 1986. Lake trout consumed significantly larger molluscs of all taxa than did round whitefish, and selected larger molluscs than were available on either rocky or soft-sediment habitats. Round whitefish were not size-selective on the snail Lymnaea, but were size-selective on the snail Valvata and on clams from the soft sediments. Round whitefish consumed fewer and smaller Lymnaea compared to lake trout. Because lake trout ate more Lymnaea and also tended to select larger, reproductive-sized individuals, this fish could potentially have a more detrimental impact on the Lymnaea population. Finally, differences in Lymnaea densities and size distributions between lakes with and without lake trout suggest that these fish may be responsible for the pattern of distribution, size, and density observed for Lymnaea in Toolik Lake and other area lakes.     

Spatial variation of shell morphometrics in the subantarctic land snail <Emphasis Type="Italic">Notodiscus hookeri</Emphasis> from Crozet and Kerguelen Islands

The land snail Notodiscus hookeri, widely distributed in subantarctic islands, shows a large intraspecific variation in shell morphology. In the present work, shell size and form of individuals from populations located in Crozet and Kerguelen archipelagos were investigated by means of multivariate statistics. Variation in shell morphometrics was analysed after the partitioning of the overall variation into size and shape components by means of a principal component-based approach. Shell size shows a significant spatial heterogeneity, which seems essentially related to environmental pressures. Previous works pointed to a greater conchological variation between populations from Kerguelen but present observations show that intra-island variances are not significantly different in the two islands studied. Variation in shell shape splits the populations into two main entities because of different allometric relationships between two shell height components and all other measurements. However, using geographical affinities of populations as instrumental variables shows that more complex environmental features interfered in population clustering.     

Factors affecting the distribution and abundance of the commensal <Emphasis Type="Italic">Temnocephala iheringi</Emphasis> (Platyhelminthes: Temnocephalidae) among the southernmost populations of the apple snail <Emphasis Type="Italic">Pomacea canaliculata </Emphasis>(Mollusca: Ampullariidae)

Temnocephala iheringi is the most common temnocephalan inhabiting the mantle cavity of the apple snail Pomacea canaliculata, a freshwater neotropical gastropod that has become a serious rice pest in Southeastern Asia. T. iheringi has been recorded from Mato Grosso (Brazil) to water bodies associated with the Río de la Plata river (Argentina). During an extensive survey in the southern limit of the native area of P.␣canaliculata the presence of T. iheringi eggs was recorded in several apple snail populations, extending the known distribution of the commensal more than 400 km southwards. The aim of this study was to understand the factors affecting the distribution and abundance of T. iheringi among populations of P.␣canaliculata. Only 23% of the apple snail populations inhabiting streams harboured temnocephalans while the occurrence among lentic ones was 71%. T. iheringi was found mostly in populations of apple snails living in non-alkaline sites and where snails attaining sizes larger than 4 cm were very common. The prevalence of the temnocephalans in lentic populations was higher than 90%. The number of eggs on the shell (not including the umbilicus) ranged between 0 and 470 and was different among populations of P.␣canaliculata. The prevalence and number of eggs were lower in the lotic populations, except for a stream population immediately downstream of a lake with commensals. There was no difference between males and females of P. canaliculata neither in the prevalence nor in the number of eggs on the shell. The southernmost population of the world of P. canaliculata harbours commensals that tolerate cold winter water temperatures (4–5 °C) as well as its host. On the other hand, T. iheringi was found only in sites with bicarbonate concentrations lower than 6.6 meq l⁻¹, suggesting that the tolerance of the commensal is very much lower than that of the apple snail (up to 9.95 meq l⁻¹). The number of worms inside each snail or the life history variation of P. canaliculata could explain the influence of the size of the snails on the occurrence of T. iheringi. In the big-sized snails, where the number of commensals is higher, the probability of survival of at least one worm is also higher, specially during the hibernation period, when crawling and feeding are null and snails remain buried. On the other hand, P. canaliculata snails from lentic populations are generally bigger and mostly iteroparous, while those inhabiting streams are smaller and semelparous. In these populations the snails have access to mate only with snails of their same cohort, while in iteroparous populations they can copulate with individuals of other cohorts, allowing the inter-generation transmission of worms and the long term persistence of the population of commensals.     

A layover in Europe: Reconstructing the invasion route of asexual lineages of a New Zealand snail to North America

Non‐native invasive species are threatening ecosystems and biodiversity worldwide. High genetic variation is thought to be a critical factor for invasion success. Accordingly, the global invasion of a few clonal lineages of the gastropod Potamopyrgus antipodarum is thus both puzzling and has the potential to help illuminate why some invasions succeed while others fail. Here, we used SNP markers and a geographically broad sampling scheme (N = 1617) including native New Zealand populations and invasive North American and European populations to provide the first widescale population genetic assessment of the relationships between and among native and invasive P. antipodarum. We used a combination of traditional and Bayesian molecular analyses to demonstrate that New Zealand populations harbour very high diversity relative to the invasive populations and are the source of the two main European genetic lineages. One of these two European lineages was in turn the source of at least one of the two main North American genetic clusters of invasive P. antipodarum, located in Lake Ontario. The other widespread North American group had a more complex origin that included the other European lineage and two New Zealand clusters. Altogether, our analyses suggest that just a small handful of clonal lineages of P. antipodarum were responsible for invasion across continents. Our findings provide critical information for prevention of additional invasions and control of existing invasive populations and are of broader relevance towards understanding the establishment and evolution of asexual populations and the forces driving biological invasion.     

Lake Superior: an invasion coldspot?

Lake Superior receives a disproportionate number of ballast water discharges from transoceanic ships operating on the Laurentian Great Lakes. Although this provides dispersal opportunities for nonindigenous species (NIS), relatively few NIS were initially discovered in this lake prior to being recorded elsewhere in the basin. A lack of NIS records from this lake may be an artefact of sampling bias. We tested this hypothesis by sampling benthos and plankton from littoral and deepwater habitats around the perimeter of Lake Superior during June and August 2001. Using morphological analysis techniques, we identified a total of 230 invertebrate taxa representing planktonic, benthic and nektonic lifestyles. Five species with invasion histories in the lower Great Lakes, the bivalves Sphaerium corneum, Pisidium amnicum and P. moitessierianum, gastropod Potamopyrgus antipodarum and amphipod Echinogammarus ischnus, were identified for the first time in Lake Superior. In addition, records of expanded distributions within this lake are presented for the amphipod Gammarus fasciatus and oligochaetes Ripistes parasita and Vejdovskyella intermedia. Recently introduced NIS in Lake Superior were found near international ports, implicating shipping as the vector of their introduction. Intrinsic physical-chemical aspects of Lake Superior may account for the scarcity of NIS in this lake as compared to the lower Great Lakes.     

First Record of Podonominae Larvae Living Phoretically on the Shells of the Water Snail Chilina dombeyana (Diptera: Chironomidae / Gastropoda: Lymnaeidae)

Larvae of Podonomus albinervis Edwards, 1931 were found phoretic on Gastropoda Chilina dombeyana (Bruigière, 1789) on the shores of Lake Nahuel Huapi, in Bariloche, Argentina. Larvae were attached with mucus and some had developed a tube made of detritus on the spire of the snail shell. Adults and pupae with associated larval exuviae were found, which helped to identify the species. Approximately 10% of the snail individuals examined on the shores of the lake had chironomid larvae on their shells. Laboratory observations showed that the midge larvae leave the snail shell when the snail leaves the water, thus demonstrating the phoretic relationship. The high density of both snails and Chironomidae in the littoral habitats of the lake may explain this phoretic relationship.     

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.     

Disentangling the effects of intraspecies variability,phylogeny, space,and climate on the evolution of shell morphology in endemic Greek land snails of the genus Codringtonia

Extensive variation in land snail shell morphology has been widely documented, although few studies have attempted to investigate the ecological and evolutionary drivers of this variation. Within a comparative phylogenetic framework, we investigated the temporal and spatial evolution of the shell morphology of the Greek endemic land snail genus Codringtonia. The contribution of both inter‐ and intraspecies shell differentiation in the overall shell variability is assessed. The effect of climate, space, and evolutionary history on the shell variability was inferred using a variance partitioning framework. For Codringtonia species, intraspecies divergence of shell traits contributes substantially to the overall shell variability. By decomposing this variability, it was shown that the overall shell size of Codringtonia clades is phylogenetically constrained, related to early speciation events, and strongly affected by large‐scale spatial variability (latitudinal gradient). The effect of climate on shell size cannot be disentangled from phylogeny and space. Shell and, to a larger extent, aperture shape are not phylogenetically constrained, and appear to be mostly related to conspecific populations divergence events. Shell shape is substantially explained by both climate and space that greatly overlap. Aperture shape is mainly interpreted by medium to small‐scale spatial variables. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 796–813.