Propensity for selfing varies within a population of hermaphroditic snails: coexistence of selfers, outcrossers and mixed-mating individuals.

To understand mating-system evolution in self-compatible hermaphrodites, variation in selfing rates is highly relevant. Empirical studies are rarely designed to capture variation between individuals, instead often comparing species and populations. Yet, evolution primarily occurs within populations, rendering among-individual variation essential. Observed individual selfing rates depend on the environment (e.g. differences in mate availability) and individuals' propensity for selfing. We quantified individual variation in selfing propensity in the snail Radix balthica by conducting laboratory mating trials that manipulated mate availability (low versus moderate) and estimating selfing rates from progeny arrays. We also measured female lifetime fitness. We found substantial among-individual variation in selfing propensity, including pure selfers (32%), pure outcrossers (31%) and mixed-mating individuals that selfed and outcrossed (37%). Experimental levels of mate availability did not significantly affect selfing rates. Selfers had reduced female liftetime fitness. Our results show that the propensity for selfing can differ considerably among individuals, with similar proportions of selfers, outcrossers and mixed maters. As mate availability did not affect selfing, our 'moderate' experimental level of mate availability might still have been too low to prompt selfers to outcross. This and the observed fitness differences also cautiously suggest that investigating the heritability of selfing propensities might be worthwhile in this population.

The evolutionary ecology of fungal killer phenotypes.

Ecological interactions influence evolutionary dynamics by selecting upon fitness variation within species. Antagonistic interactions often promote genetic and species diversity, despite the inherently suppressive effect they can have on the species experiencing them. A central aim of evolutionary ecology is to understand how diversity is maintained in systems experiencing antagonism. In this review, we address how certain single-celled and dimorphic fungi have evolved allelopathic killer phenotypes that engage in antagonistic interactions. We discuss the evolutionary pathways to the production of lethal toxins, the functions of killer phenotypes and the consequences of competition for toxin producers, their competitors and toxin-encoding endosymbionts. Killer phenotypes are powerful models because many appear to have evolved independently, enabling across-phylogeny comparisons of the origins, functions and consequences of allelopathic antagonism. Killer phenotypes can eliminate host competitors and influence evolutionary dynamics, yet the evolutionary ecology of killer phenotypes remains largely unknown. We discuss what is known and what remains to be ascertained about killer phenotype ecology and evolution, while bringing their model system properties to the reader's attention.

Parasite infection and the movement of the aquatic snail Potamopyrgus antipodarum along a depth cline.

Parasite species that use two or more host species during their life cycle depend on successful transmission between these species. These successive host species may have different habitat requirements. For example, one host species may be aquatic while the other is terrestrial. To overcome this complicating factor in transmission, a wide diversity of parasite species have adaptations that alter the habitat preference in one host species to facilitate transmission to the next host species.Two common trematode parasites in New Zealand, Atriophallophorus winterbourni and Notocotylus spp., both have a life cycle with two host species. The aquatic snail Potamopyrgus antipodarum is the intermediate host, from which the parasites require transmission to dabbling ducks or other waterfowl. Of these parasites, A. winterbourni is most frequently found in snails from the shallow-water margin. This may indicate parasite-induced movement of infected snails into the foraging habitat of dabbling ducks.To test whether the parasites manipulate the snails to move into shallow water, we stretched tubular mesh cages across depth-specific ecological habitat zones in a lake. Both infected and healthy snails were released into the cages. After 11 days, significantly higher infection frequencies of A. winterbourni were retrieved from the shallowest end of the cages, while Notocotylus spp. frequencies did not vary with depth.The hypothesis that A. winterbourni induces its snail host to move into the shallow-water habitat cannot be rejected based on the experimental results. Although further research is needed to address alternative explanations, the depth preference of infected snails may be due to a parasite adaptation that facilitates trophic transmission of parasites to dabbling ducks.

Ornaments indicate parasite load only if they are dynamic or parasites are contagious.

Choosing to mate with an infected partner has several potential fitness costs, including disease transmission and infection-induced reductions in fecundity and parental care. By instead choosing a mate with no, or few, parasites, animals avoid these costs and may also obtain resistance genes for offspring. Within a population, then, the quality of sexually selected ornaments on which mate choice is based should correlate negatively with the number of parasites with which a host is infected ("parasite load"). However, the hundreds of tests of this prediction yield positive, negative, or no correlation between parasite load and ornament quality. Here, we use phylogenetically controlled meta-analysis of 424 correlations from 142 studies on a wide range of host and parasite taxa to evaluate explanations for this ambiguity. We found that ornament quality is weakly negatively correlated with parasite load overall, but the relationship is more strongly negative among ornaments that can dynamically change in quality, such as behavioral displays and skin pigmentation, and thus can accurately reflect current parasite load. The relationship was also more strongly negative among parasites that can transmit during sex. Thus, the direct benefit of avoiding parasite transmission may be a key driver of parasite-mediated sexual selection. No other moderators, including methodological details and whether males exhibit parental care, explained the substantial heterogeneity in our data set. We hope to stimulate research that more inclusively considers the many and varied ways in which parasites, sexual selection, and epidemiology intersect.

Sensitivity of bipartite network analyses to incomplete sampling and taxonomic uncertainty.

Bipartite network analysis is a powerful tool to study the processes structuring interactions in ecological communities. In applying the method, it is assumed that the sampled interactions provide an accurate representation of the actual community. However, acquiring a representative sample may be difficult as not all species are equally abundant or easily identifiable. Two potential sampling issues can compromise the conclusions of bipartite network analyses: failure to capture the full range of interactions (sampling completeness) and use of a taxonomic level higher than species to evaluate the network (taxonomic resolution). We asked how commonly used descriptors of bipartite antagonistic communities (modularity, nestedness, connectance, and specialization [H2 ']) are affected by reduced host sampling completeness, parasite taxonomic resolution, and their crossed effect, as they are likely to co-occur. We used a quantitative niche model to generate weighted bipartite networks that resembled natural host-parasite communities. The descriptors were more sensitive to uncertainty in parasite taxonomic resolution than to host sampling completeness. When only 10% of parasite taxonomic resolution was retained, modularity and specialization decreased by ~76% and ~12%, respectively, and nestedness and connectance increased by ~114% and ~345% respectively. The loss of taxonomic resolution led to a wide range of possible communities, which made it difficult to predict its effects on a given network. With regards to host sampling completeness, standardized nestedness, connectance, and specialization were robust, whereas modularity was sensitive (~30% decrease). The combination of both sampling issues had an additive effect on modularity. In communities with low effort for both sampling issues (50%-10% of sampling completeness and taxonomic resolution), estimators of modularity, and nestedness could not be distinguished from those of random assemblages. Thus, the categorical description of communities with low sampling effort (e.g., if a community is modular or not) should be done with caution. We recommend evaluating both sampling completeness and taxonomic certainty when conducting bipartite network analyses. Care should also be exercised when using nonrobust descriptors (the four descriptors for parasite taxonomic resolution; modularity for host sampling completeness) when sampling issues are likely to affect a dataset.

Phylogeography and cryptic species structure of a locally adapted parasite in New Zealand.

The phylogeographic patterns of many taxa on New Zealand's South Island are characterized by disjunct distributions that have been attributed to Pleistocene climatic cycles and the formation of the Southern Alps. Pleistocene glaciation has been implicated in shaping the contemporary genetic differentiation between populations of the aquatic snail Potamopyrgus antipodarum. We investigated whether similar phylogeographic patterns exist for the snail's locally adapted trematode parasite, Atriophallophorus winterbourni. We found evidence for a barrier to gene-flow in sympatry between cryptic, but ecologically divergent species. When focusing on the most common of these species, disjunct geographic distributions are found for mitochondrial lineages that diverged during the Pleistocene. The boundary between these distributions is found in the central part of the South Island and is reinforced by low cross-alpine migration. Further support for a vicariant origin of the phylogeographic pattern was found when assessing nuclear multilocus SNP data. Nuclear and mitochondrial population differentiation was concordant in pattern, except for populations in a potential secondary contact zone. Additionally, we found larger than expected differentiation between nuclear- and mitochondrial-based empirical Bayes FST estimates (global FST : 0.02 vs. 0.39 for nuclear and mitochondrial data, respectively). Population subdivision is theoretically expected to be stronger for mitochondrial genomes due to a smaller effective population size, but the strong difference here, together with mitonuclear discordance in a putative contact zone, is potentially indicative of divergent gene flow of nuclear and mitochondrial genomes.

Scent of a killer: How could killer yeast boost its dispersal?

Vector-borne parasites often manipulate hosts to attract uninfected vectors. For example, parasites causing malaria alter host odor to attract mosquitoes. Here, we discuss the ecology and evolution of fruit-colonizing yeast in a tripartite symbiosis-the so-called "killer yeast" system. "Killer yeast" consists of Saccharomyces cerevisiae yeast hosting two double-stranded RNA viruses (M satellite dsRNAs, L-A dsRNA helper virus). When both dsRNA viruses occur in a yeast cell, the yeast converts to lethal toxin­producing "killer yeast" phenotype that kills uninfected yeasts. Yeasts on ephemeral fruits attract insect vectors to colonize new habitats. As the viruses have no extracellular stage, they depend on the same insect vectors as yeast for their dispersal. Viruses also benefit from yeast dispersal as this promotes yeast to reproduce sexually, which is how viruses can transmit to uninfected yeast strains. We tested whether insect vectors are more attracted to killer yeasts than to non­killer yeasts. In our field experiment, we found that killer yeasts were more attractive to Drosophila than non-killer yeasts. This suggests that vectors foraging on yeast are more likely to transmit yeast with a killer phenotype, allowing the viruses to colonize those uninfected yeast strains that engage in sexual reproduction with the killer yeast. Beyond insights into the basic ecology of the killer yeast system, our results suggest that viruses could increase transmission success by manipulating the insect vectors of their host.

Gene Duplication and Gain in the Trematode Atriophallophorus winterbourni Contributes to Adaptation to Parasitism.

Gene duplications and novel genes have been shown to play a major role in helminth adaptation to a parasitic lifestyle because they provide the novelty necessary for adaptation to a changing environment, such as living in multiple hosts. Here we present the de novo sequenced and annotated genome of the parasitic trematode Atriophallophorus winterbourni and its comparative genomic analysis to other major parasitic trematodes. First, we reconstructed the species phylogeny, and dated the split of A. winterbourni from the Opisthorchiata suborder to approximately 237.4 Ma (±120.4 Myr). We then addressed the question of which expanded gene families and gained genes are potentially involved in adaptation to parasitism. To do this, we used hierarchical orthologous groups to reconstruct three ancestral genomes on the phylogeny leading to A. winterbourni and performed a GO (Gene Ontology) enrichment analysis of the gene composition of each ancestral genome, allowing us to characterize the subsequent genomic changes. Out of the 11,499 genes in the A. winterbourni genome, as much as 24% have arisen through duplication events since the speciation of A. winterbourni from the Opisthorchiata, and as much as 31.9% appear to be novel, that is, newly acquired. We found 13 gene families in A. winterbourni to have had more than ten genes arising through these recent duplications; all of which have functions potentially relating to host behavioral manipulation, host tissue penetration, and hiding from host immunity through antigen presentation. We identified several families with genes evolving under positive selection. Our results provide a valuable resource for future studies on the genomic basis of adaptation to parasitism and point to specific candidate genes putatively involved in antagonistic host-parasite adaptation.

Coinfecting parasites can modify fluctuating selection dynamics in host-parasite coevolution.

Genetically specific interactions between hosts and parasites can lead to coevolutionary fluctuations in their genotype frequencies over time. Such fluctuating selection dynamics are, however, expected to occur only under specific circumstances (e.g., high fitness costs of infection to the hosts). The outcomes of host-parasite interactions are typically affected by environmental/ecological factors, which could modify coevolutionary dynamics. For instance, individual hosts are often infected with more than one parasite species and interactions between them can alter host and parasite performance. We examined the potential effects of coinfections by genetically specific (i.e., coevolving) and nonspecific (i.e., generalist) parasite species on fluctuating selection dynamics using numerical simulations. We modeled coevolution (a) when hosts are exposed to a single parasite species that must genetically match the host to infect, (b) when hosts are also exposed to a generalist parasite that increases fitness costs to the hosts, and (c) when coinfecting parasites compete for the shared host resources. Our results show that coinfections can enhance fluctuating selection dynamics when they increase fitness costs to the hosts. Under resource competition, coinfections can either enhance or suppress fluctuating selection dynamics, depending on the characteristics (i.e., fecundity, fitness costs induced to the hosts) of the interacting parasites.

The Size, Symmetry, and Color Saturation of a Male Guppy's Ornaments Forecast His Resistance to Parasites.

AbstractSexually selected ornaments range from highly dynamic traits to those that are fixed during development and relatively static throughout sexual maturity. Ornaments along this continuum differ in the information they provide about the qualities of potential mates, such as their parasite resistance. Dynamic ornaments enable real-time assessment of the bearer's condition: they can reflect an individual's current infection status, or they can reflect resistance to recent infections. Static ornaments, however, are not affected by recent infection but may instead indicate an individual's genetically determined resistance, even in the absence of infection. Given the typically aggregated distribution of parasites among hosts, infection is unlikely to affect the ornaments of the vast majority of individuals in a population: static ornaments may therefore be the more reliable indicators of parasite resistance. To test this hypothesis, we quantified the ornaments of male guppies (Poecilia reticulata) before experimentally infecting them with Gyrodactylus turnbulli. Males with more left-right symmetrical black coloration and those with larger areas of orange coloration, both static ornaments, were more resistant. However, males with more saturated orange coloration, a dynamic ornament, were less resistant. Female guppies often prefer symmetrical males with larger orange ornaments, suggesting that parasite-mediated natural and sexual selection act in concert on these traits.

Stream microbial communities and ecosystem functioning show complex responses to multiple stressors in wastewater.

Multiple anthropogenic drivers are changing ecosystems globally, with a disproportionate and intensifying impact on freshwater habitats. A major impact of urbanization are inputs from wastewater treatment plants (WWTPs). Initially designed to reduce eutrophication and improve water quality, WWTPs increasingly release a multitude of micropollutants (MPs; i.e., synthetic chemicals) and microbes (including antibiotic-resistant bacteria) to receiving environments. This pollution may have pervasive impacts on biodiversity and ecosystem services. Viewed through multiple lenses of macroecological and ecotoxicological theory, we combined field, flume, and laboratory experiments to determine the effects of wastewater (WW) on microbial communities and organic-matter processing using a standardized decomposition assay. First, we conducted a mensurative experiment sampling 60 locations above and below WWTP discharges in 20 Swiss streams. Microbial respiration and decomposition rates were positively influenced by WW inputs via warming and nutrient enrichment, but with a notable exception: WW decreased the activation energy of decomposition, indicating a "slowing" of this fundamental ecosystem process in response to temperature. Second, next-generation sequencing indicated that microbial community structure below WWTPs was altered, with significant compositional turnover, reduced richness, and evidence of negative MP influences. Third, a series of flume experiments confirmed that although diluted WW generally has positive influences on microbial-mediated processes, the negative effects of MPs are "masked" by nutrient enrichment. Finally, transplant experiments suggested that WW-borne microbes enhance decomposition rates. Taken together, our results affirm the multiple stressor paradigm by showing that different aspects of WW (warming, nutrients, microbes, and MPs) jointly influence ecosystem functioning in complex ways. Increased respiration rates below WWTPs potentially generate ecosystem "disservices" via greater carbon evasion from streams and rivers. However, toxic MP effects may fundamentally alter ecological scaling relationships, indicating the need for a rapprochement between ecotoxicological and macroecological perspectives.

On biological evolution and environmental solutions.

Drawing insights from multiple disciplines is essential for finding integrative solutions that are required to tackle complex environmental problems. Human activities are causing unprecedented influence on global ecosystems, culminating in the loss of species and fundamental changes in the selective environments of organisms across the tree of life. Our collective understanding about biological evolution can help identify and mitigate many of the environmental problems in the Anthropocene. To this end, we propose a stronger integration of environmental sciences with evolutionary biology.

Inbreeding does not alter the response to an experimental heat wave in a freshwater snail.

Global climate change affects natural populations of many species by increasing the average temperature and the frequency of extreme weather events (e.g. summer heat waves). The ability of organisms to cope with these environmental changes can, however, depend on their genetic properties. For instance, genetic load owing to inbreeding could alter organisms' responses to climate change-mediated environmental changes but such effects are often overlooked. We investigated the effects of an experimental heat wave (25°C versus 15°C) on life history (reproduction, size) and constitutive immune defence traits (phenoloxidase-like and antibacterial activity of haemolymph) in relation to inbreeding by manipulating the mating type (outcrossing, self-fertilization) in two populations of a hermaphroditic freshwater snail, Lymnaea stagnalis. High temperature increased reproduction and size of snails but impaired their immune function. In one of the two study populations, inbreeding reduced reproductive output of snails indicating inbreeding depression. Furthermore, this effect did not depend on the temperature snails were exposed to. Our results suggest that L. stagnalis snails can be negatively affected by inbreeding but it may not alter their responses to heat waves.

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.

Dissimilarity of individual microsatellite profiles under different mutation models: Empirical approach.

Microsatellites (simple sequence repeats, SSRs) still remain popular molecular markers for studying neutral genetic variation. Two alternative models outline how new microsatellite alleles evolve. Infinite alleles model (IAM) assumes that all possible alleles are equally likely to result from a mutation, while stepwise mutation model (SMM) describes microsatellite evolution as stepwise adding or subtracting single repeat units. Genetic relationships between individuals can be analyzed in higher precision when assuming the SMM scenario with allele size differences as a proxy of genetic distance. If population structure is not predetermined in advance, an empirical data analysis usually includes (a) estimating proximity between individual SSR profiles with a selected dissimilarity measure and (b) determining putative genetic structure of a given set of individuals using methods of clustering and/or ordination for the obtained dissimilarity matrix. We developed new dissimilarity indices between SSR profiles of haploid, diploid, or polyploid organisms assuming different mutation models and compared the performance of these indices for determining genetic structure with population data and with simulations. More specifically, we compared SMM with a constant or variable mutation rate at different SSR loci to IAM using data from natural populations of a freshwater bryozoan Cristatella mucedo (diploid), wheat leaf rust Puccinia triticina (dikaryon), and wheat powdery mildew Blumeria graminis (monokaryon). We show that inferences about population genetic structure are sensitive to the assumed mutation model. With simulations, we found that Bruvo's distance performs generally poorly, while the new metrics are capturing the differences in the genetic structure of the populations.

The role of plasticity in the evolution of cryptic pigmentation in a freshwater isopod.

Cryptic pigmentation of prey is often thought to evolve in response to predator-mediated selection, but pigmentation traits can also be plastic, and change with respect to both abiotic and biotic environmental conditions. In such cases, identifying the presence of, and drivers of trait plasticity is useful for understanding the evolution of crypsis. Previous work suggests that cryptic pigmentation of freshwater isopods (Asellus aquaticus) has evolved in response to predation pressure by fish in habitats with varying macrophyte cover and coloration. However, macrophytes can potentially influence the distribution of pigmentation by altering not only habitat-specific predation susceptibility, but also dietary resources and abiotic conditions. The goals of this study were to experimentally test how two putative agents of selection, namely macrophytes and fish, affect the pigmentation of A. aquaticus, and to assess whether pigmentation is plastic, using a diet manipulation in a common garden. We performed two experiments: (a) in an outdoor mesocosm experiment, we investigated how different densities of predatory fish (0/30/60 three-spined stickleback [Gasterosteus aculeatus] per mesocosm) and macrophytes (presence/absence) affected the abundance, pigmentation and body size structure of isopod populations. (b) In a subsequent laboratory experiment, we reared isopods in a common garden experiment on two different food sources (high/low protein content) to test whether variation in pigmentation of isopods can be explained by diet-based developmental plasticity. We found that fish presence strongly reduced isopod densities, particularly in the absence of macrophytes, but had no effect on pigmentation or size structure of the populations. However, we found that isopods showed consistently higher pigmentation in the presence of macrophytes, regardless of fish presence or absence. Our laboratory experiment, in which we manipulated the protein content of the isopods' diet, revealed strong plasticity of pigmentation and weak plasticity of growth rate. The combined results of both experiments suggest that pigmentation of A. aquaticus is a developmentally plastic trait and that multiple environmental factors (e.g. macrophytes, diet and predation) might jointly influence the evolution of cryptic pigmentation of A. aquaticus in nature on relatively short time-scales.

Importance of Sequence and Timing in Parasite Coinfections.

Coinfections by multiple parasites predominate in the wild. Interactions between parasites can be antagonistic, neutral, or facilitative, and they can have significant implications for epidemiology, disease dynamics, and evolution of virulence. Coinfections commonly result from sequential exposure of hosts to different parasites. We argue that the sequential nature of coinfections is important for the consequences of infection in both natural and man-made environments. Coinfections accumulate during host lifespan, determining the structure of the parasite infracommunity. Interactions within the parasite community and their joint effect on the host individual potentially shape evolution of parasite life-history traits and transmission biology. Overall, sequential coinfections have the potential to change evolutionary and epidemiological outcomes of host-parasite interactions widely across plant and animal systems.

Estimating species distribution and abundance in river networks using environmental DNA.

All organisms leave traces of DNA in their environment. This environmental DNA (eDNA) is often used to track occurrence patterns of target species. Applications are especially promising in rivers, where eDNA can integrate information about populations upstream. The dispersion of eDNA in rivers is modulated by complex processes of transport and decay through the dendritic river network, and we currently lack a method to extract quantitative information about the location and density of populations contributing to the eDNA signal. Here, we present a general framework to reconstruct the upstream distribution and abundance of a target species across a river network, based on observed eDNA concentrations and hydro-geomorphological features of the network. The model captures well the catchment-wide spatial biomass distribution of two target species: a sessile invertebrate (the bryozoan Fredericella sultana) and its parasite (the myxozoan Tetracapsuloides bryosalmonae). Our method is designed to easily integrate general biological and hydrological data and to enable spatially explicit estimates of the distribution of sessile and mobile species in fluvial ecosystems based on eDNA sampling.

Integrated field, laboratory, and theoretical study of PKD spread in a Swiss prealpine river.

Proliferative kidney disease (PKD) is a major threat to wild and farmed salmonid populations because of its lethal effect at high water temperatures. Its causative agent, the myxozoan Tetracapsuloides bryosalmonae, has a complex lifecycle exploiting freshwater bryozoans as primary hosts and salmonids as secondary hosts. We carried out an integrated study of PKD in a prealpine Swiss river (the Wigger). During a 3-year period, data on fish abundance, disease prevalence, concentration of primary hosts' DNA in environmental samples [environmental DNA (eDNA)], hydrological variables, and water temperatures gathered at various locations within the catchment were integrated into a newly developed metacommunity model, which includes ecological and epidemiological dynamics of fish and bryozoans, connectivity effects, and hydrothermal drivers. Infection dynamics were captured well by the epidemiological model, especially with regard to the spatial prevalence patterns. PKD prevalence in the sampled sites for both young-of-the-year (YOY) and adult brown trout attained 100% at the end of summer, while seasonal population decay was higher in YOY than in adults. We introduce a method based on decay distance of eDNA signal predicting local species' density, accounting for variation in environmental drivers (such as morphology and geology). The model provides a whole-network overview of the disease prevalence. In this study, we show how spatial and environmental characteristics of river networks can be used to study epidemiology and disease dynamics of waterborne diseases.