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.

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.

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.

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.

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.

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.

Increase in multiple paternity across the reproductive lifespan in a sperm-storing, hermaphroditic freshwater snail.

Polyandry is a common phenomenon and challenges the traditional view of stronger sexual selection in males than in females. In simultaneous hermaphrodites, the physical proximity of both sex functions was long thought to preclude the operation of sexual selection. Laboratory studies suggest that multiple mating and polyandry in hermaphrodites may actually be common, but data from natural populations are sparse. We therefore estimated the rate of multiple paternity and its seasonal variability in the annual, sperm-storing, simultaneously hermaphroditic freshwater snail Radix balthica for the entire duration of the reproductive lifespan. We also tested whether multiple paternity was associated with clutch size or embryonic development. To obtain these data, we measured and genotyped 60 field-collected egg clutches using nine highly polymorphic microsatellite markers. Overall, 50% of the clutches had multiple fathers, and both the frequency (20-93% of clutches) and magnitude of multiple paternity (mean 1.3-3.8 fathers per clutch) substantially increased over time, probably because of extensive sperm storage. Most multiply sired clutches (83%) had a dominant father, but neither clutch size nor the proportion of developed embryos per clutch was associated with levels of multiple paternity. Both the evident promiscuity and the frequent skew of paternity shares suggest that sexual selection may be an important evolutionary force in the study population.

Fine-Scale Spatial Covariation between Infection Prevalence and Susceptibility in a Natural Population.

The prevalence of infection varies dramatically on a fine spatial scale. Many evolutionary hypotheses are founded on the assumption that this variation is due to host genetics, such that sites with a high frequency of alleles conferring susceptibility are associated with higher infection prevalence. This assumption is largely untested and may be compromised at finer spatial scales where gene flow between sites is high. We put this assumption to the test in a natural snail-trematode interaction in which host susceptibility is known to have a strong genetic basis. A decade of field sampling revealed substantial spatial variation in infection prevalence between 13 sites around a small lake. Laboratory assays replicated over 3 years demonstrate striking variation in host susceptibility among sites in spite of high levels of gene flow between sites. We find that mean susceptibility can explain more than one-third of the observed variation in mean infection prevalence among sites. We estimate that variation in susceptibility and exposure together can explain the majority of variation in prevalence. Overall, our findings in this natural host-parasite system argue that spatial variation in infection prevalence covaries strongly with variation in the distribution of genetically based susceptibility, even at a fine spatial scale.

Interactions among bacterial strains and fluke genotypes shape virulence of co-infection.

Most studies of virulence of infection focus on pairwise host-parasite interactions. However, hosts are almost universally co-infected by several parasite strains and/or genotypes of the same or different species. While theory predicts that co-infection favours more virulent parasite genotypes through intensified competition for host resources, knowledge of the effects of genotype by genotype (G × G) interactions between unrelated parasite species on virulence of co-infection is limited. Here, we tested such a relationship by challenging rainbow trout with replicated bacterial strains and fluke genotypes both singly and in all possible pairwise combinations. We found that virulence (host mortality) was higher in co-infections compared with single infections. Importantly, we also found that the overall virulence was dependent on the genetic identity of the co-infecting partners so that the outcome of co-infection could not be predicted from the respective virulence of single infections. Our results imply that G × G interactions among co-infecting parasites may significantly affect host health, add to variance in parasite fitness and thus influence evolutionary dynamics and ecology of disease in unexpected ways.

Trends in self-reported sleep problems, tiredness and related school performance among Finnish adolescents from 1984 to 2011.

The aim of this study was to investigate long-term trends in insomnia symptoms, tiredness and school performance among Finnish adolescents. A time-series from 1984 to 2011 was analysed from two large-scale survey studies, the Finnish School Health Promotion Study and the Health Behavior in School-Aged Children study. A total of 1,136,583 adolescents aged 11-18 years answered a standardized questionnaire assessing frequency of insomnia symptoms, tiredness and school performance. A clear approximately twofold increasing trend in insomnia symptoms and tiredness was found from the mid-1990s to the end of the 2000s. The increase was evident in all participating age groups and in both genders. After 2008, the increase seems to have stopped. Insomnia symptoms and tiredness were associated with lower school performance and they were more prevalent among girls (11.9 and 18.4%) compared to boys (6.9 and 9.0%, respectively). Unexpectedly, we also observed an increasingly widening gap in school performance between normally vigilant and chronically tired pupils. The underlying causes of these phenomena are unknown, but may concern changes in the broader society. The observed recent increasing trend in adolescents' sleep problems is worrisome: poor sleep quality has also been suggested to associate with clinical or subclinical mood or anxiety disorders and behavioural problems and predispose to sleep and psychiatric disorders later in life. Our results justify further studies and call for serious attention to be paid to adolescent's sleep in the Finnish educational system and society at large.

Infection dynamics in coexisting sexual and asexual host populations: support for the Red Queen hypothesis.

The persistence of sexual reproduction is a classic problem in evolutionary biology. The problem stems from the fact that, all else equal, asexual lineages should rapidly replace coexisting sexual individuals due to the cost of producing males in sexual populations. One possible countervailing advantage to sexual reproduction is that, on average, outcrossed offspring are more resistant than common clones to coevolving parasites, as predicted under the Red Queen hypothesis. In this study, we evaluated the prevalence of infection by a sterilizing trematode (Microphallus sp.) in a natural population of freshwater snails that was composed of both sexual and asexual individuals (Potamopyrgus antipodarum). More specifically, we compared the frequency of infection in sexual and asexual individuals over a 5-year period at four sites at a natural glacial lake (Lake Alexandrina, South Island, New Zealand). We found that at most sites and over most years, the sexual population was less infected than the coexisting asexual population. Moreover, the frequency of uninfected sexual females was periodically greater than two times the frequency of uninfected asexual females. These results give clear support for a fluctuating parasite-mediated advantage to sexual reproduction in a natural population.

Evolutionary demography of agricultural expansion in preindustrial northern Finland.

A shift from nomadic foraging to sedentary agriculture was a major turning point in human evolutionary history, increasing our population size and eventually leading to the development of modern societies. We however lack understanding of the changes in life histories that contributed to the increased population growth rate of agriculturalists, because comparable individual-based reproductive records of sympatric populations of agriculturalists and foragers are rarely found. Here, we compared key life-history traits and population growth rate using comprehensive data from the seventieth to nineteenth century Northern Finland: indigenous Sami were nomadic hunter-fishers and reindeer herders, whereas sympatric agricultural Finns relied predominantly on animal husbandry. We found that agriculture-based families had higher lifetime fecundity, faster birth spacing and lower maternal mortality. Furthermore, agricultural Finns had 6.2% higher annual population growth rate than traditional Sami, which was accounted by differences between the subsistence modes in age-specific fecundity but not in mortality. Our results provide, to our knowledge, the most detailed demonstration yet of the demographic changes and evolutionary benefits that resulted from agricultural revolution.

Large variation in mitochondrial DNA of sexual and parthenogenetic Dahlica triquetrella (Lepidoptera: Psychidae) shows multiple origins of parthenogenesis.

BACKGROUND: Obligate parthenogenesis is relatively rare in animals. Still, in some groups it is quite common and has evolved and persisted multiple times. These groups may provide important clues to help solve the 'paradox of sex'. Several species in the Psychidae (Lepidoptera) have obligate parthenogenesis. Dahlica triquetrella is one of those species where multiple transitions to parthenogenesis are postulated based on intensive cytological and behavioural studies. This has led to the hypothesis that multiple transitions from sexuals to diploid parthenogens occurred during and after the last glacial period, followed by transitions from parthenogenetic diploids to parthenogenetic tetraploids. Our study is the first to test these hypotheses using a molecular phylogeny based on mtDNA from multiple sexual and parthenogenetic populations from a wide geographic range. RESULTS: Parthenogenetic (and sexual) D. triquetrella are not monophyletic, and considerable sequence variation is present suggesting multiple transitions to parthenogenesis. However, we could not establish ancestral sexual haplotypes from our dataset. Our data suggest that some parthenogenetic clades have evolved, indicating origins of parthenogenesis before the last glacial period. CONCLUSIONS: Multiple transitions to parthenogenesis have taken place in Dahlica triquetrella, confirming previous hypotheses. The number of different parthenogenetic clades, haplotypes and their apparent evolutionary age, clearly show that parthenogenesis has been a very successful reproductive strategy in this species over a long period.

The geographic mosaic of sex and infection in lake populations of a New Zealand snail at multiple spatial scales.

Understanding how sexual and asexual forms of the same species coexist is a challenge for evolutionary biology. The Red Queen hypothesis predicts that sex is favored by parasite-mediated selection against common asexual genotypes, leading to the coexistence of sexual and asexual hosts. In a geographic mosaic, where the risk of infection varies in space, the theory also predicts that sexual reproduction would be positively correlated with disease prevalence. We tested this hypothesis in lake populations of a New Zealand freshwater snail, Potamopyrgus antipodarum, by comparing pairwise difference matrices for infection frequency and male frequency using partial Mantel tests. We conducted the test at three spatial scales: among lakes on the South Island, among depths within an intensively sampled lake (Lake Alexandrina), and within depths at Lake Alexandrina. We found that the difference in infection risk and the difference in the proportion of sexual snails were significantly and positively correlated at all spatial scales. Our results thus suggest that parasite-mediated selection contributes to the long-term coexistence of sexual and asexual individuals in coevolutionary hotspots, and that the "warmth" of hotspots can vary on small spatial scales.

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.

Prevalence of infection as a predictor of multiple genotype infection frequency in parasites with multiple-host life cycle.

In nature, parasites commonly share hosts with other conspecific parasite genotypes. While adult parasites typically show aggregated distribution in their final hosts, aggregation of clonal parasite genotypes in intermediate hosts, such as those of trematodes in molluscs, is not generally known. However, infection of a host by multiple parasite genotypes has significant implications for evolution of virulence and host-parasite coevolution. Aggregated distribution of the clonal stages can increase host mortality and reduce larval output of each infecting genotype through interclonal competition, and therefore have significant implications for parasite epidemiology. The aim of this study was (i) to find out how common multiple genotype infections (MGIs) are in aquatic snails serving as intermediate hosts for different trematode species; (ii) to find out whether the prevalence of infection could be used to predict MGI frequencies and (iii) to use the relationship to infer whether MGIs aggregate in molluscan hosts. We determined the prevalence of trematode (Diplostomum pseudospathaceum) infections and the frequency of MGIs in snail (Lymnaea stagnalis) host populations as well as compiled corresponding literature data from a range of snail-trematode systems. We used Bayesian simulations to explore the relationship between prevalence of infection and MGI frequency in these data, and tested whether genotypes aggregate in snails by comparing the simulated relations with null model (Poisson and demographic Poisson) expectations. Our results show that MGIs are common in aquatic snails with up to 90% of the infected snails carrying MGIs. Parasite prevalence is a good predictor of MGI frequencies at a range of prevailing natural prevalences of infection (0-50%). The frequency of MGIs was higher than expected by both null models, indicating parasite aggregation at genotype level. These findings are in sharp contrast with the absence of multiple infections in snails at level of trematode species, suggesting that co-infections by multiple species and multiple genotypes of one species are controlled by different biological processes. Aggregation of MGIs in snail hosts appears to be widespread across different snail-trematode systems.

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.

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.

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.