A longitudinal survey in the wild reveals major shifts in fish host microbiota after parasite infection.

Recent studies have highlighted associations between diseases and host microbiota. It remains extremely challenging - especially under natural conditions - to clarify whether host microbiota promote future infections, or whether changes in host microbiota result from infections. Nonetheless, deciphering between these two processes is essential for highlighting the role of microbes in disease progression. We longitudinally surveyed, in the wild, the microbiota of individual fish hosts (Leuciscus burdigalensis) both before and after infection by a crustacean ectoparasite (Tracheliastes polycolpus). We found a striking association between parasite infection and the host microbiota composition restricted to the fins the parasite anchored. We clearly demonstrated that infections by the parasite induced a shift in (and did not result from) the host fin microbiota. Furthermore during infection, the microbiota of infected fins got similar to the microbiota of the adult stage, and the free-living infective stage of the parasite with a predominance of the Burkholderiaceae bacteria family. This suggests that some Burkholderiaceae bacteria are involved in a coinfection process and possibly facilitate T. polycolpus infection. In this study, we reveal novel mechanistic insights for understanding the role of the microbiota in host-parasite interactions, which has implications for predicting the progression of diseases in natural host populations.

Historical dispersal and host-switching formed the evolutionary history of a globally distributed multi-host parasite - The Ligula intestinalis species complex.

Studies on parasite biogeography and host spectrum provide insights into the processes driving parasite diversification. Global geographical distribution and a multi-host spectrum make the tapeworm Ligula intestinalis a promising model for studying both the vicariant and ecological modes of speciation in parasites. To understand the relative importance of host association and biogeography in the evolutionary history of this tapeworm, we analysed mtDNA and reduced-represented genomic SNP data for a total of 139 specimens collected from 18 fish-host genera across a distribution range representing 21 countries. Our results strongly supported the existence of at least 10 evolutionary lineages and estimated the deepest divergence at approximately 4.99-5.05 Mya, which is much younger than the diversification of the fish host genera and orders. Historical biogeography analyses revealed that the ancestor of the parasite diversified following multiple vicariance events and was widespread throughout the Palearctic, Afrotropical, and Nearctic between the late Miocene and early Pliocene. Cyprinoids were inferred as the ancestral hosts for the parasite. Later, from the late Pliocene to Pleistocene, new lineages emerged following a series of biogeographic dispersal and host-switching events. Although only a few of the current Ligula lineages show narrow host-specificity (to a single host genus), almost no host genera, even those that live in sympatry, overlapped between different Ligula lineages. Our analyses uncovered the impact of historical distribution shifts on host switching and the evolution of host specificity without parallel host-parasite co-speciation. Historical biogeography reconstructions also found that the parasite colonized several areas (Afrotropical and Australasian) much earlier than was suggested by only recent faunistic data.

Inferring Causalities in Landscape Genetics: An Extension of Wright's Causal Modeling to Distance Matrices.

Identifying landscape features that affect functional connectivity among populations is a major challenge in fundamental and applied sciences. Landscape genetics combines landscape and genetic data to address this issue, with the main objective of disentangling direct and indirect relationships among an intricate set of variables. Causal modeling has strong potential to address the complex nature of landscape genetic data sets. However, this statistical approach was not initially developed to address the pairwise distance matrices commonly used in landscape genetics. Here, we aimed to extend the applicability of two causal modeling methods-that is, maximum-likelihood path analysis and the directional separation test-by developing statistical approaches aimed at handling distance matrices and improving functional connectivity inference. Using simulations, we showed that these approaches greatly improved the robustness of the absolute (using a frequentist approach) and relative (using an information-theoretic approach) fits of the tested models. We used an empirical data set combining genetic information on a freshwater fish species (Gobio occitaniae) and detailed landscape descriptors to demonstrate the usefulness of causal modeling to identify functional connectivity in wild populations. Specifically, we demonstrated how direct and indirect relationships involving altitude, temperature, and oxygen concentration influenced within- and between-population genetic diversity of G. occitaniae.

Systematic conservation planning for intraspecific genetic diversity.

Intraspecific diversity informs the demographic and evolutionary histories of populations, and should be a main conservation target. Although approaches exist for identifying relevant biological conservation units, attempts to identify priority conservation areas for intraspecific diversity are scarce, especially within a multi-specific framework. We used neutral molecular data on six European freshwater fish species (Squalius cephalus, Phoxinus phoxinus, Barbatula barbatula, Gobio occitaniae, Leuciscus burdigalensis and Parachondrostoma toxostoma) sampled at the riverscape scale (i.e. the Garonne-Dordogne river basin, France) to determine hot- and coldspots of genetic diversity, and to identify priority conservation areas using a systematic conservation planning approach. We demonstrate that systematic conservation planning is efficient for identifying priority areas representing a predefined part of the total genetic diversity of a whole landscape. With the exception of private allelic richness (PA), classical genetic diversity indices (allelic richness, genetic uniqueness) were poor predictors for identifying priority areas. Moreover, we identified weak surrogacies among conservation solutions found for each species, implying that conservation solutions are highly species-specific. Nonetheless, we showed that priority areas identified using intraspecific genetic data from multiple species provide more effective conservation solutions than areas identified for single species or on the basis of traditional taxonomic criteria.

Catch-related and genetic outcome of adult northern pike Esox lucius stocking in a large river system.

Genetic introgression from stocked adult northern pike Esox lucius to a wild self-recruiting population was detected in a large river system and some stocked E. lucius survived up to two spawning seasons and dispersed over several kilometres in the river. Moreover, the catch rate of stocked E. lucius by anglers was low (9.6%), hence suggesting that the efficiency of stocking activity is questionable.

Host dispersal as the driver of parasite genetic structure: a paradigm lost?

Understanding traits influencing the distribution of genetic diversity has major ecological and evolutionary implications for host-parasite interactions. The genetic structure of parasites is expected to conform to that of their hosts, because host dispersal is generally assumed to drive parasite dispersal. Here, we used a meta-analysis to test this paradigm and determine whether traits related to host dispersal correctly predict the spatial co-distribution of host and parasite genetic variation. We compiled data from empirical work on local adaptation and host-parasite population genetic structure from a wide range of taxonomic groups. We found that genetic differentiation was significantly lower in parasites than in hosts, suggesting that dispersal may often be higher for parasites. A significant correlation in the pairwise genetic differentiation of hosts and parasites was evident, but surprisingly weak. These results were largely explained by parasite reproductive mode, the proportion of free-living stages in the parasite life cycle and the geographical extent of the study; variables related to host dispersal were poor predictors of genetic patterns. Our results do not dispel the paradigm that parasite population genetic structure depends on host dispersal. Rather, we highlight that alternative factors are also important in driving the co-distribution of host and parasite genetic variation.

Local adaptation drives thermal tolerance among parasite populations: a common garden experiment.

Understanding the evolutionary responses of organisms to thermal regimes is of prime importance to better predict their ability to cope with ongoing climate change. Although this question has attracted interest in free-living organisms, whether or not infectious diseases have evolved heterogeneous responses to climate is still an open question. Here, we ran a common garden experiment using the fish ectoparasite Tracheliastes polycolpus, (i) to test whether parasites living in thermally heterogeneous rivers respond differently to an experimental thermal gradient and (ii) to determine the evolutionary processes (natural selection or genetic drift) underlying these responses. We demonstrated that the reaction norms involving the survival rate of the parasite larvae (i.e. the infective stage) across a temperature gradient significantly varied among six parasite populations. Using a Qst/Fst approach and phenotype-environment associations, we further showed that the evolution of survival rate partly depended upon temperature regimes experienced in situ, and was mostly underlined by diversifying selection, but also-to some extent-by stabilizing selection and genetic drift. This evolutionary response led to population divergences in thermal tolerance across the landscape, which has implications for predicting the effects of future climate change.

Elucidating the spatio-temporal dynamics of an emerging wildlife pathogen using approximate Bayesian computation.

Emerging pathogens constitute a severe threat for human health and biodiversity. Determining the status (native or non-native) of emerging pathogens, and tracing back their spatio-temporal dynamics, is crucial to understand the eco-evolutionary factors promoting their emergence, to control their spread and mitigate their impacts. However, tracing back the spatio-temporal dynamics of emerging wildlife pathogens is challenging because (i) they are often neglected until they become sufficiently abundant and pose socio-economical concerns and (ii) their geographical range is often little known. Here, we combined classical population genetics tools and approximate Bayesian computation (i.e. ABC) to retrace the dynamics of Tracheliastes polycolpus, a poorly documented pathogenic ectoparasite emerging in Western Europe that threatens several freshwater fish species. Our results strongly suggest that populations of T. polycolpus in France emerged from individuals originating from a unique genetic pool that were most likely introduced in the 1920s in central France. From this initial population, three waves of colonization occurred into peripheral watersheds within the next two decades. We further demonstrated that populations remained at low densities, and hence undetectable, during 10 years before a major demographic expansion occurred, and before its official detection in France. These findings corroborate and expand the few historical records available for this emerging pathogen. More generally, our study demonstrates how ABC can be used to determine the status, reconstruct the colonization history and infer key evolutionary parameters of emerging wildlife pathogens with low data availability, and for which samples from the putative native area are inaccessible.

Heritable variation in host tolerance and resistance inferred from a wild host-parasite system.

Hosts have evolved two distinct defence strategies against parasites: resistance (which prevents infection or limit parasite growth) and tolerance (which alleviates the fitness consequences of infection). However, heritable variation in resistance and tolerance and the genetic correlation between these two traits have rarely been characterized in wild host populations. Here, we estimate these parameters for both traits in Leuciscus burdigalensis, a freshwater fish parasitized by Tracheliastes polycolpus. We used a genetic database to construct a full-sib pedigree in a wild L. burdigalensis population. We then used univariate animal models to estimate inclusive heritability (i.e. all forms of genetic and non-genetic inheritance) in resistance and tolerance. Finally, we assessed the genetic correlation between these two traits using a bivariate animal model. We found significant heritability for resistance (H = 17.6%; 95% CI: 7.2-32.2%) and tolerance (H = 18.8%; 95% CI: 4.4-36.1%), whereas we found no evidence for the existence of a genetic correlation between these traits. Furthermore, we confirm that resistance and tolerance are strongly affected by environmental effects. Our results demonstrate that (i) heritable variation exists for parasite resistance and tolerance in wild host populations, and (ii) these traits can evolve independently in populations.

When does a parasite become a disease? eDNA unravels complex host-pathogen dynamics across environmental stress gradients in wild salmonid populations.

Infectious diseases stem from disrupted interactions among hosts, parasites, and the environment. Both abiotic and biotic factors can influence infection outcomes by shaping the abundance of a parasite's infective stages, as well as the host's ability to fight infection. However, disentangling these mechanisms within natural ecosystems remains challenging. Here, combining environmental DNA analysis and niche modelling at a regional scale, we uncovered the biotic and abiotic drivers of an infectious disease of salmonid fish, triggered by the parasite Tetracapsuloides bryosalmonae. We found that the occurrence and abundance of the parasite in the water-i.e., the propagule pressure- were mainly correlated to the abundances of its two primary hosts, the bryozoan Fredericella sultana and the fish Salmo trutta, but poorly to local abiotic environmental stressors. In contrast, the occurrence and abundance of parasites within fish hosts-i.e., proxies for disease emergence-were closely linked to environmental stressors (water temperature, agricultural activities, dams), and to a lesser extent to parasite propagule pressure. These results suggest that pathogen distribution alone cannot predict the risk of disease in wildlife, and that local anthropogenic stressors may play a pivotal role in disease emergence among wild host populations, likely by modulating the hosts' immune response. Our study sheds light on the intricate interplay between biotic and abiotic factors in shaping pathogen distribution and raises concerns about the effects of global change on pathogen emergence.

Optimizing detectability of the endangered fan mussel using eDNA and ddPCR.

Spatial and temporal monitoring of species threatened with extinction is of critical importance for conservation and ecosystem management. In the Mediterranean coast, the fan mussel (Pinna nobilis) is listed as critically endangered after suffering from a mass mortality event since 2016, leading to 100% mortality in most marine populations. Conventional monitoring for this macroinvertebrate is done using scuba, which is challenging in dense meadows or with low visibility. Here we developed an environmental DNA assay targeting the fan mussel and assessed the influence of several environmental parameters on the species detectability in situ. We developed and tested an eDNA molecular marker and collected 48 water samples in two sites at the Thau lagoon (France) with distinct fan mussel density, depths and during two seasons (summer and autumn). Our marker can amplify fan mussel DNA but lacks specificity since it also amplifies a conspecific species (Pinna rudis). We successfully amplified fan mussel DNA from in situ samples with 46 positive samples (out of 48) using ddPCR, although the DNA concentrations measured were low over almost all samples. Deeper sampling depth slightly increased DNA concentrations, but no seasonal effect was found. We highlight a putative spawning event on a single summer day with much higher DNA concentration compared to all other samples. We present an eDNA molecular assay able to detect the endangered fan mussel and provide guidelines to optimize the sampling protocol to maximize detectability. Effective and non-invasive monitoring tools for endangered species are promising to monitor remaining populations and have the potential of ecological restoration or habitat recolonization following a mass mortality event.

Genetic erosion reduces biomass temporal stability in wild fish populations.

Genetic diversity sustains species adaptation. However, it may also support key ecosystems functions and services, for example biomass production, that can be altered by the worldwide loss of genetic diversity. Despite extensive experimental evidence, there have been few attempts to empirically test whether genetic diversity actually promotes biomass and biomass stability in wild populations. Here, using long-term demographic wild fish data from two large river basins in southwestern France, we demonstrate through causal modeling analyses that populations with high genetic diversity do not reach higher biomasses than populations with low genetic diversity. Nonetheless, populations with high genetic diversity have much more stable biomasses over recent decades than populations having suffered from genetic erosion, which has implications for the provision of ecosystem services and the risk of population extinction. Our results strengthen the importance of adopting prominent environmental policies to conserve this important biodiversity facet.

Transcriptomic Adjustments in a Freshwater Ectoparasite Reveal the Role of Molecular Plasticity for Parasite Host Shift.

A parasite's lifestyle is characterized by a critical dependency on its host for feeding, shelter and/or reproduction. The ability of parasites to exploit new host species can reduce the risk associated with host dependency. The number of host species that can be infected by parasites strongly affects their ecological and evolutionary dynamics along with their pathogenic effects on host communities. However, little is known about the processes and the pathways permitting parasites to successfully infect alternative host species, a process known as host shift. Here, we tested whether molecular plasticity changes in gene expression and in molecular pathways could favor host shift in parasites. Focusing on an invasive parasite, Tracheliastes polycolpus, infecting freshwater fish, we conducted a transcriptomic study to compare gene expression in parasites infecting their main host species and two alternative host species. We found 120 significant differentially expressed genes (DEGs) between parasites infecting the different host species. A total of 90% of the DEGs were identified between parasites using the main host species and those using the two alternative host species. Only a few significant DEGs (seven) were identified when comparing parasites from the two alternative host species. Molecular pathways enriched in DEGs and associated with the use of alternative host species were related to cellular machinery, energetic metabolism, muscle activity and oxidative stress. This study strongly suggests that molecular plasticity is an important mechanism sustaining the parasite's ability to infect alternative hosts.

Host characteristics and environmental factors differentially drive the burden and pathogenicity of an ectoparasite: a multilevel causal analysis.

1. Understanding the ecological factors driving the burden and pathogenicity of parasites is challenging. Indeed, the dynamics of host-parasite interactions is driven by factors organized across nested hierarchical levels (e.g. hosts, localities), and indirect effects are expected owing to interactions between levels. 2. In this study, we combined Bayesian multilevel models, path analyses and a model selection procedure to account for these complexities and to decipher the relative effects of host- and environment-related factors on the burden and the pathogenicity of an ectoparasite (Tracheliastes polycolpus) on its fish host (Leuciscus leuciscus). We also tested the year-to-year consistency of the relationships linking these factors to the burden and the pathogenic effects of T. polycolpus. 3. We found significant relationships between the parasite burden and host-related factors: body length and age were positively related to parasite burden and heterozygous hosts displayed a higher parasite burden. In contrast, both host- and environment-related factors were linked to pathogenic effects. Pathogenicity was correlated negatively with host body length and positively with age; this illustrates that some factors (e.g. body length) showed inverse relationships with parasite burden and pathogenicity. Pathogenic effects were stronger in cooler upstream sites and where host density was lower. Path analyses revealed that these relationships between environment-related factors and pathogenic effects were direct and were not indirect relationships mediated by the host characteristics. Finally, we found that the strength and the shape of certain relationships were consistent across years, while they were clearly not for some others. 4. Our study illustrates that considering conjointly causal relationships among factors and the hierarchical structure of host-parasite interactions is appropriate for dissecting the complex links between hosts, parasites and their common environment.

Patterns of Epigenetic Diversity in Two Sympatric Fish Species: Genetic vs. Environmental Determinants.

Epigenetic components are hypothesized to be sensitive to the environment, which should permit species to adapt to environmental changes. In wild populations, epigenetic variation should therefore be mainly driven by environmental variation. Here, we tested whether epigenetic variation (DNA methylation) observed in wild populations is related to their genetic background, and/or to the local environment. Focusing on two sympatric freshwater fish species (Gobio occitaniae and Phoxinus phoxinus), we tested the relationships between epigenetic differentiation, genetic differentiation (using microsatellite and single nucleotide polymorphism (SNP) markers), and environmental distances between sites. We identify positive relationships between pairwise genetic and epigenetic distances in both species. Moreover, epigenetic marks better discriminated populations than genetic markers, especially in G. occitaniae. In G. occitaniae, both pairwise epigenetic and genetic distances were significantly associated to environmental distances between sites. Nonetheless, when controlling for genetic differentiation, the link between epigenetic differentiation and environmental distances was not significant anymore, indicating a noncausal relationship. Our results suggest that fish epigenetic variation is mainly genetically determined and that the environment weakly contributed to epigenetic variation. We advocate the need to control for the genetic background of populations when inferring causal links between epigenetic variation and environmental heterogeneity in wild populations.

Molecular approaches reveal weak sibship aggregation and a high dispersal propensity in a non-native fish parasite.

Inferring parameters related to the aggregation pattern of parasites and to their dispersal propensity are important for predicting their ecological consequences and evolutionary potential. Nonetheless, it is notoriously difficult to infer these parameters from wildlife parasites given the difficulty in tracking these organisms. Molecular-based inferences constitute a promising approach that has yet rarely been applied in the wild. Here, we combined several population genetic analyses including sibship reconstruction to document the genetic structure, patterns of sibship aggregation, and the dispersal dynamics of a non-native parasite of fish, the freshwater copepod ectoparasite Tracheliastes polycolpus. We collected parasites according to a hierarchical sampling design, with the sampling of all parasites from all host individuals captured in eight sites spread along an upstream-downstream river gradient. Individual multilocus genotypes were obtained from 14 microsatellite markers, and used to assign parasites to full-sib families and to investigate the genetic structure of T. polycolpus among both hosts and sampling sites. The distribution of full-sibs obtained among the sampling sites was used to estimate individual dispersal distances within families. Our results showed that T. polycolpus sibs tend to be aggregated within sites but not within host individuals. We detected important upstream-to-downstream dispersal events of T. polycolpus between sites (modal distance: 25.4 km; 95% CI [22.9, 27.7]), becoming scarcer as the geographic distance from their family core location increases. Such a dispersal pattern likely contributes to the strong isolation-by-distance observed at the river scale. We also detected some downstream-to-upstream dispersal events (modal distance: 2.6 km; 95% CI [2.2-23.3]) that likely result from movements of infected hosts. Within each site, the dispersal of free-living infective larvae among hosts likely contributes to increasing genetic diversity on hosts, possibly fostering the evolutionary potential of T. polycolpus.

Stable resource polymorphism along the benthic littoral-pelagic axis in an invasive crayfish.

Although intraspecific variability is now widely recognized as affecting evolutionary and ecological processes, our knowledge on the importance of intraspecific variability within invasive species is still limited. This is despite the fact that understanding the linkage between within-population morphological divergences and the use of different trophic or spatial resources (i.e., resource polymorphism) can help to better predict their ecological impacts on recipient ecosystems. Here, we quantified the extent of resource polymorphism within populations of a worldwide invasive crayfish species, Procambarus clarkii, in 16 lake populations by comparing their trophic (estimated using stable isotope analyses) and morphological characteristics between individuals from the littoral and pelagic habitats. Our results first demonstrated that crayfish occured in both littoral and pelagic habitats of seven lakes and that the use of pelagic habitat was associated with increased abundance of littoral crayfish. We then found morphological (i.e., body and chelae shapes) and trophic divergence (i.e., reliance on littoral carbon) among individuals from littoral and pelagic habitats, highlighting the existence of resource polymorphism in invasive populations. There was no genetic differentiation between individuals from the two habitats, implying that this resource polymorphism was stable (i.e., high gene flow between individuals). Finally, we demonstrated that a divergent adaptive process was responsible for the morphological divergence in body and chela shapes between habitats while difference in littoral reliance neutrally evolved under genetic drift. These findings demonstrated that invasive P. clarkii can display strong within-population phenotypic variability in recent populations, and this could lead to contrasting ecological impacts between littoral and pelagic individuals.

Quantifying the individual impact of artificial barriers in freshwaters: A standardized and absolute genetic index of fragmentation.

Fragmentation by artificial barriers is an important threat to freshwater biodiversity. Mitigating the negative aftermaths of fragmentation is of crucial importance, and it is now essential for environmental managers to benefit from a precise estimate of the individual impact of weirs and dams on river connectivity. Although the indirect monitoring of fragmentation using molecular data constitutes a promising approach, it is plagued with several constraints preventing a standardized quantification of barrier effects. Indeed, observed levels of genetic differentiation GD depend on both the age of the obstacle and the effective size of the populations it separates, making comparisons of the actual barrier effect of different obstacles difficult. Here, we developed a standardized genetic index of fragmentation (F INDEX), allowing an absolute and independent assessment of the individual effects of obstacles on connectivity. The F INDEX is the standardized ratio between the observed GD between pairs of populations located on either side of an obstacle and the GD expected if this obstacle completely prevented gene flow. The expected GD is calculated from simulations taking into account two parameters: the number of generations since barrier creation and the expected heterozygosity of the populations, a proxy for effective population size. Using both simulated and empirical datasets, we explored the validity and the limits of the F INDEX. We demonstrated that it allows quantifying effects of fragmentation only from a few generations after barrier creation and provides valid comparisons among obstacles of different ages and populations (or species) of different effective sizes. The F INDEX requires a minimum amount of fieldwork and genotypic data and solves some of the difficulties inherent to the study of artificial fragmentation in rivers and potentially in other ecosystems. This makes the F INDEX promising to support the management of freshwater species affected by barriers, notably for planning and evaluating restoration programs.

A river runs through it: The causes, consequences, and management of intraspecific diversity in river networks.

Rivers are fascinating ecosystems in which the eco-evolutionary dynamics of organisms are constrained by particular features, and biologists have developed a wealth of knowledge about freshwater biodiversity patterns. Over the last 10 years, our group used a holistic approach to contribute to this knowledge by focusing on the causes and consequences of intraspecific diversity in rivers. We conducted empirical works on temperate permanent rivers from southern France, and we broadened the scope of our findings using experiments, meta-analyses, and simulations. We demonstrated that intraspecific (genetic) diversity follows a spatial pattern (downstream increase in diversity) that is repeatable across taxa (from plants to vertebrates) and river systems. This pattern can result from interactive processes that we teased apart using appropriate simulation approaches. We further experimentally showed that intraspecific diversity matters for the functioning of river ecosystems. It indeed affects not only community dynamics, but also key ecosystem functions such as litter degradation. This means that losing intraspecific diversity in rivers can yield major ecological effects. Our work on the impact of multiple human stressors on intraspecific diversity revealed that-in the studied river systems-stocking of domestic (fish) strains strongly and consistently alters natural spatial patterns of diversity. It also highlighted the need for specific analytical tools to tease apart spurious from actual relationships in the wild. Finally, we developed original conservation strategies at the basin scale based on the systematic conservation planning framework that appeared pertinent for preserving intraspecific diversity in rivers. We identified several important research avenues that should further facilitate our understanding of patterns of local adaptation in rivers, the identification of processes sustaining intraspecific biodiversity-ecosystem function relationships, and the setting of reliable conservation plans.

Evidence of parasite-mediated disruptive selection on genetic diversity in a wild fish population.

Identifying the processes maintaining genetic variability in wild populations is a major concern in conservation and evolutionary biology. Parasite-mediated selection may strongly affect genetic variability in wild populations. The inbreeding depression theory predicts that directional selection imposed by parasites should act against the most inbred hosts, thus favouring genetic diversity in wild populations. We have tested this prediction by evaluating the strength and shape of the relationship between the load of a harmful fin-feeder ectoparasite (Tracheliastes polycolpus) and the genome-wide genetic diversity (i.e. heterozygosity measured at a set of 15 microsatellites) of its fish host, the rostrum dace (Leuciscus leuciscus). Contrary to expectation, we found a nonlinear relationship between host genetic diversity and ectoparasite load, with hosts that were either homozygous or heterozygous harbouring significantly fewer parasites than hosts with an intermediate level of heterozygosity. This relationship suggests that parasites could increase the variance of global heterozygosity in this host population through disruptive selection on genetic diversity. Moreover, when genetic diversity was measured at each locus separately, we found two very strong positive associations between host genetic diversity and the ectoparasite load. This latter result has three main implications: (i) genome-wide effect cannot alone explain the nonlinear relationship between global heterozygosity and ectoparasite load, (ii) negative non-additive allelic interactions (i.e. underdominance) may be a mechanism for resisting ectoparasite infection, and (iii) ectoparasites may favour homozygosity at some loci in this host population.