Parasite-mediated predation determines infection in a complex predator-prey-parasite system.

The interplay of host-parasite and predator-prey interactions is critical in ecological dynamics because both predators and parasites can regulate communities. But what is the prevalence of infected prey and predators when a parasite is transmitted through trophic interactions considering stochastic demographic changes? Here, we modelled and analysed a complex predator-prey-parasite system, where parasites are transmitted from prey to predators. We varied parasite virulence and infection probabilities to investigate how those evolutionary factors determine species' coexistence and populations' composition. Our results show that parasite species go extinct when the infection probabilities of either host are small and that success in infecting the final host is more critical for the survival of the parasite. While our stochastic simulations are consistent with deterministic predictions, stochasticity plays an important role in the border regions between coexistence and extinction. As expected, the proportion of infected individuals increases with the infection probabilities. Interestingly, the relative abundances of infected and uninfected individuals can have opposite orders in the intermediate and final host populations. This counterintuitive observation shows that the interplay of direct and indirect parasite effects is a common driver of the prevalence of infection in a complex system.

Host habitat rather than evolutionary history explains gut microbiome diversity in sympatric stickleback species.

Host-associated microbiota can influence host phenotypic variation, fitness and potential to adapt to local environmental conditions. In turn, both host evolutionary history and the abiotic and biotic environment can influence the diversity and composition of microbiota. Yet, to what extent environmental and host-specific factors drive microbial diversity remains largely unknown, limiting our understanding of host-microbiome interactions in natural populations. Here, we compared the intestinal microbiota between two phylogenetically related fishes, the three-spined stickleback (Gasterosteus aculeatus) and the nine-spined stickleback (Pungitius pungitius) in a common landscape. Using amplicon sequencing of the V3-V4 region of the bacterial 16S rRNA gene, we characterised the α and ß diversity of the microbial communities in these two fish species from both brackish water and freshwater habitats. Across eight locations, α diversity was higher in the nine-spined stickleback, suggesting a broader niche use in this host species. Habitat was a strong determinant of ß diversity in both host species, while host species only explained a small fraction of the variation in gut microbial composition. Strong habitat-specific effects overruled effects of geographic distance and historical freshwater colonisation, suggesting that the gut microbiome correlates primarily with local environmental conditions. Interestingly, the effect of habitat divergence on gut microbial communities was stronger in three-spined stickleback than in nine-spined stickleback, possibly mirroring the stronger level of adaptive divergence in this host species. Overall, our results show that microbial communities reflect habitat divergence rather than colonisation history or dispersal limitation of host species.

Origin matters: Using a local reference genome improves measures in population genomics.

Genome sequencing enables answering fundamental questions about the genetic basis of adaptation, population structure and epigenetic mechanisms. Yet, we usually need a suitable reference genome for mapping population-level resequencing data. In some model systems, multiple reference genomes are available, giving the challenging task of determining which reference genome best suits the data. Here, we compared the use of two different reference genomes for the three-spined stickleback (Gasterosteus aculeatus), one novel genome derived from a European gynogenetic individual and the published reference genome of a North American individual. Specifically, we investigated the impact of using a local reference versus one generated from a distinct lineage on several common population genomics analyses. Through mapping genome resequencing data of 60 sticklebacks from across Europe and North America, we demonstrate that genetic distance among samples and the reference genomes impacts downstream analyses. Using a local reference genome increased mapping efficiency and genotyping accuracy, effectively retaining more and better data. Despite comparable distributions of the metrics generated across the genome using SNP data (i.e. π, Tajima's D and FST ), window-based statistics using different references resulted in different outlier genes and enriched gene functions. A marker-based analysis of DNA methylation distributions had a comparably high overlap in outlier genes and functions, yet with distinct differences depending on the reference genome. Overall, our results highlight how using a local reference genome decreases reference bias to increase confidence in downstream analyses of the data. Such results have significant implications in all reference-genome-based population genomic analyses.

Context-dependent parasite infection affects trophic niche in populations of sympatric stickleback species.

How parasites alter host feeding ecology remains elusive in natural populations. A powerful approach to investigate the link between infection and feeding ecology is quantifying unique and shared responses to parasite infection in related host species within a common environment. Here, 9 pairs of sympatric populations of the three-spined and nine-spined stickleback fishes were sampled across a range of freshwater and brackish habitats to investigate how parasites alter host feeding ecology: (i) biotic and abiotic determinants of parasite community composition, and (ii) to what extent parasite infection correlates with trophic niche specialization of the 2 species, using stable isotope analyses (δ15N and δ13C). It was determined that parasite community composition and host parasite load varied among sites and species and were correlated with dissolved oxygen. It was also observed that the digenean Cyathocotyle sp.'s abundance, a common directly infecting parasite with a complex life cycle, correlated with host δ13C in a fish species-specific manner. In 6 sites, correlations were found between parasite abundance and their hosts' feeding ecology. These effects were location-specific and occasionally host species or host size-specific. Overall, the results suggest a relationship between parasite infection and host trophic niche which may be an important and largely overlooked ecological factor. The population specificity and variation in parasite communities also suggest this effect is multifarious and context-dependent.

Divergent and non-parallel evolution of MHC IIB in the Neotropical Midas cichlid species complex.

BACKGROUND: Ecological diversification is the result of divergent natural selection by contrasting habitat characteristics that favours the evolution of distinct phenotypes. This process can happen in sympatry and in allopatry. Habitat-specific parasite communities have the potential to drive diversification among host populations by imposing selective pressures on their host's immune system. In particular, the hyperdiverse genes of the major histocompatibility complex (MHC) are implicated in parasite-mediated host divergence. Here, we studied the extent of divergence at MHC, and discuss how it may have contributed to the Nicaraguan Midas cichlid species complex diversification, one of the most convincing examples of rapid sympatric parallel speciation. RESULTS: We genotyped the MHC IIB for individuals from six sympatric Midas cichlid assemblages, each containing species that have adapted to exploit similar habitats. We recovered large allelic and functional diversity within the species complex. While most alleles were rare, functional groups of alleles (supertypes) were common, suggesting that they are key to survival and that they were maintained during colonization and subsequent radiations. We identified lake-specific and habitat-specific signatures for both allelic and functional diversity, but no clear pattern of parallel divergence among ecomorphologically similar phenotypes. CONCLUSIONS: Colonization and demographic effects of the fish could have contributed to MHC evolution in the Midas cichlid in conjunction with habitat-specific selective pressures, such as parasites associated to alternative preys or environmental features. Additional ecological data will help evaluating the role of host-parasite interactions in the Midas cichlid radiations and aid in elucidating the potential role of non-parallel features differentiating crater lake species assemblages.

Effects of global warming on species with temperature-dependent sex determination: Bridging the gap between empirical research and management.

Global warming could threaten over 400 species with temperature-dependent sex determination (TSD) worldwide, including all species of sea turtle. During embryonic development, rising temperatures might lead to the overproduction of one sex and, in turn, could bias populations' sex ratios to an extent that threatens their persistence. If climate change predictions are correct, and biased sex ratios reduce population viability, species with TSD may go rapidly extinct unless adaptive mechanisms, whether behavioural, physiological or molecular, exist to buffer these temperature-driven effects. Here, we summarize the discovery of the TSD phenomenon and its still elusive evolutionary significance. We then review the molecular pathways underpinning TSD in model species, along with the hormonal mechanisms that interact with temperatures to determine an individual's sex. To illustrate evolutionary mechanisms that can affect sex determination, we focus on sea turtle biology, discussing both the adaptive potential of this threatened TSD taxon, and the risks associated with conservation mismanagement.

Distribution of genetic diversity reveals colonization patterns and philopatry of the loggerhead sea turtles across geographic scales.

Understanding the processes that underlie the current distribution of genetic diversity in endangered species is a goal of modern conservation biology. Specifically, the role of colonization and dispersal events throughout a species' evolutionary history often remains elusive. The loggerhead sea turtle (Caretta caretta) faces multiple conservation challenges due to its migratory nature and philopatric behaviour. Here, using 4207 mtDNA sequences, we analysed the colonisation patterns and distribution of genetic diversity within a major ocean basin (the Atlantic), a regional rookery (Cabo Verde Archipelago) and a local island (Island of Boa Vista, Cabo Verde). Data analysis using hypothesis-driven population genetic models suggests the colonization of the Atlantic has occurred in two distinct waves, each corresponding to a major mtDNA lineage. We propose the oldest lineage entered the basin via the isthmus of Panama and sequentially established aggregations in Brazil, Cabo Verde and in the area of USA and Mexico. The second lineage entered the Atlantic via the Cape of Good Hope, establishing colonies in the Mediterranean Sea, and from then on, re-colonized the already existing rookeries of the Atlantic. At the Cabo Verde level, we reveal an asymmetric gene flow maintaining links across island-specific nesting groups, despite significant genetic structure. This structure stems from female philopatric behaviours, which could further be detected by weak but significant differentiation amongst beaches separated by only a few kilometres on the island of Boa Vista. Exploring biogeographic processes at diverse geographic scales improves our understanding of the complex evolutionary history of highly migratory philopatric species. Unveiling the past facilitates the design of conservation programmes targeting the right management scale to maintain a species' evolutionary potential.

Long-term survey of sea turtles (Caretta caretta) reveals correlations between parasite infection, feeding ecology, reproductive success and population dynamics.

Long-term monitoring of host-parasite interactions is important for understanding the consequences of infection on host fitness and population dynamics. In an eight-year survey of the loggerhead sea turtle (Caretta caretta) population nesting in Cabo Verde, we determined the spatiotemporal variation of Ozobranchus margoi, a sanguivorous leech best known as a vector for sea turtle fibropapilloma virus. We quantified O. margoi association with turtles' δ15N and δ13C stable isotopes to identify where infection occurs. We then measured the influence of infection on reproduction and offspring fitness. We found that parasite prevalence has increased from 10% of the population in 2010, to 33% in 2017. Stable isotope analysis of host skin samples suggests transmission occurs within the host's feeding grounds. Interestingly, we found a significant interaction between individual size and infection on the reproductive success of turtles. Specifically, small, infected females produced fewer offspring of poorer condition, while in contrast, large, infected turtles produced greater clutch sizes and larger offspring. We interpret this interaction as evidence, upon infection, for a size-dependent shift in reproductive strategy from bet hedging to terminal investment, altering population dynamics. This link between infection and reproduction underscores the importance of using long-term monitoring to quantify the impact of disease dynamics over time.

Experimental Parasite Infection Causes Genome-Wide Changes in DNA Methylation.

Parasites are arguably among the strongest drivers of natural selection, constraining hosts to evolve resistance and tolerance mechanisms. Although, the genetic basis of adaptation to parasite infection has been widely studied, little is known about how epigenetic changes contribute to parasite resistance and eventually, adaptation. Here, we investigated the role of host DNA methylation modifications to respond to parasite infections. In a controlled infection experiment, we used the three-spined stickleback fish, a model species for host-parasite studies, and their nematode parasite Camallanus lacustris. We showed that the levels of DNA methylation are higher in infected fish. Results furthermore suggest correlations between DNA methylation and shifts in key fitness and immune traits between infected and control fish, including respiratory burst and functional trans-generational traits such as the concentration of motile sperm. We revealed that genes associated with metabolic, developmental, and regulatory processes (cell death and apoptosis) were differentially methylated between infected and control fish. Interestingly, genes such as the neuropeptide FF receptor 2 and the integrin alpha 1 as well as molecular pathways including the Th1 and Th2 cell differentiation were hypermethylated in infected fish, suggesting parasite-mediated repression mechanisms of immune responses. Altogether, we demonstrate that parasite infection contributes to genome-wide DNA methylation modifications. Our study brings novel insights into the evolution of vertebrate immunity and suggests that epigenetic mechanisms are complementary to genetic responses against parasite-mediated selection.

Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation.

Epigenetic inheritance has been proposed to contribute to adaptation and acclimation via two information channels: (i) inducible epigenetic marks that enable transgenerational plasticity and (ii) noninducible epigenetic marks resulting from random epimutations shaped by selection. We studied both postulated channels by sequencing methylomes and genomes of Baltic three-spined sticklebacks (Gasterosteus aculeatus) along a salinity cline. Wild populations differing in salinity tolerance revealed differential methylation (pop-DMS) at genes enriched for osmoregulatory processes. A two-generation experiment demonstrated that 62% of these pop-DMS were noninducible by salinity manipulation, suggesting that they are the result of either direct selection or associated genomic divergence at cis- or trans-regulatory sites. Two-thirds of the remaining inducible pop-DMS increased in similarity to patterns detected in wild populations from corresponding salinities. The level of similarity accentuated over consecutive generations, indicating a mechanism of transgenerational plasticity. While we can attribute natural DNA methylation patterns to the two information channels, their interplay with genomic variation in salinity adaptation is still unresolved.

Estimates for energy expenditure in free-living animals using acceleration proxies: A reappraisal.

It is fundamentally important for many animal ecologists to quantify the costs of animal activities, although it is not straightforward to do so. The recording of triaxial acceleration by animal-attached devices has been proposed as a way forward for this, with the specific suggestion that dynamic body acceleration (DBA) be used as a proxy for movement-based power. Dynamic body acceleration has now been validated frequently, both in the laboratory and in the field, although the literature still shows that some aspects of DBA theory and practice are misunderstood. Here, we examine the theory behind DBA and employ modelling approaches to assess factors that affect the link between DBA and energy expenditure, from the deployment of the tag, through to the calibration of DBA with energy use in laboratory and field settings. Using data from a range of species and movement modes, we illustrate that vectorial and additive DBA metrics are proportional to each other. Either can be used as a proxy for energy and summed to estimate total energy expended over a given period, or divided by time to give a proxy for movement-related metabolic power. Nonetheless, we highlight how the ability of DBA to predict metabolic rate declines as the contribution of non-movement-related factors, such as heat production, increases. Overall, DBA seems to be a substantive proxy for movement-based power but consideration of other movement-related metrics, such as the static body acceleration and the rate of change of body pitch and roll, may enable researchers to refine movement-based metabolic costs, particularly in animals where movement is not characterized by marked changes in body acceleration.

Genomic footprints of a biological invasion: Introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva).

Facilitated by the intensification of global trading, the introduction and dispersal of species to areas in which they are historically non-native is nowadays common. From an evolutionary standpoint, invasions are paradoxical: not only non-native environments could be different from native ones for which introduced individuals would be ill-adapted, but also small founding population size should be associated with reduced adaptive potential. As such, biological invasions are considered valuable real-time evolutionary experiments. Here, we investigated the population structure and adaptive potential of the highly invasive topmouth gudgeon (Pseudorasbora parva) across Europe and East Asia. We RAD-sequenced 301 specimens from sixteen populations and three distinct within-catchment invaded regions as well as two locations in the native range. With 13,785 single nucleotide polymorphisms, we provide conclusive evidence for a genome-wide signature of two distinct invasion events, in Slovakia and Turkey, each originating from a specific area in the native range. A third invaded area, in France, appears to be the result of dispersal within the invasive range. Few loci showed signs of selection, the vast majority of which being identified in the Slovakian region. Functional annotation suggests that faster early stage development, resistance to pollution and immunocompetence contribute to the invasion success of the local habitats. By showing that populations in the invasive range have different evolutionary histories, our study reinforces the idea that populations, rather than species, are the units to consider in invasion biology.

Genome-Wide Genotype-Expression Relationships Reveal Both Copy Number and Single Nucleotide Differentiation Contribute to Differential Gene Expression between Stickleback Ecotypes.

Repeated and independent emergence of trait divergence that matches habitat differences is a sign of parallel evolution by natural selection. Yet, the molecular underpinnings that are targeted by adaptive evolution often remain elusive. We investigate this question by combining genome-wide analyses of copy number variants (CNVs), single nucleotide polymorphisms (SNPs), and gene expression across four pairs of lake and river populations of the three-spined stickleback (Gasterosteus aculeatus). We tested whether CNVs that span entire genes and SNPs occurring in putative cis-regulatory regions contribute to gene expression differences between sticklebacks from lake and river origins. We found 135 gene CNVs that showed a significant positive association between gene copy number and gene expression, suggesting that CNVs result in dosage effects that can fuel phenotypic variation and serve as substrates for habitat-specific selection. Copy number differentiation between lake and river sticklebacks also contributed to expression differences of two immune-related genes in immune tissues, cathepsin A and GIMAP7. In addition, we identified SNPs in cis-regulatory regions (eSNPs) associated with the expression of 1,865 genes, including one eSNP upstream of a carboxypeptidase gene where both the SNP alleles differentiated and the gene was differentially expressed between lake and river populations. Our study highlights two types of mutations as important sources of genetic variation involved in the evolution of gene expression and in potentially facilitating repeated adaptation to novel environments.

An experimental test of how parasites of predators can influence trophic cascades and ecosystem functioning.

Parasites can shape the structure and function of ecosystems by influencing both the density and traits of their hosts. Such changes in ecosystems are particularly likely when the host is a predator that mediates the dynamics of trophic cascades. Here, we experimentally tested how parasite load of a small predatory fish, the threespine stickleback, can affect the occurrence and strength of trophic cascades and ecosystem functioning. In a factorial mesocosm experiment, we manipulated the density of stickleback (low vs. high), and the level of parasite load (natural vs. reduced). In addition, we used two stickleback populations from different lineages: an eastern European lineage with a more pelagic phenotype (Lake Constance) and a western European lineage with a more benthic phenotype (Lake Geneva). We found that stickleback caused trophic cascades in the pelagic but not the benthic food chain. Evidence for pelagic trophic cascades was stronger in treatments where parasite load of stickleback was reduced with an antihelmintic medication, and where fish originated from Lake Constance (i.e., the more pelagic lineage). A structural equation model revealed that differences in stickleback lineage and parasite load were most likely to impact trophic cascades via changes in the composition, rather than overall biomass, of zooplankton communities. Overall, our results provide experimental evidence that parasites of predators can influence the cascading effects of fish on lower trophic levels with consequences on ecosystem functioning.

Transgenerational plasticity and selection shape the adaptive potential of sticklebacks to salinity change.

In marine climate change research, salinity shifts have been widely overlooked. While widespread desalination effects are expected in higher latitudes, salinity is predicted to increase closer to the equator. We took advantage of the steep salinity gradient of the Baltic Sea as a space-for-time design to address effects of salinity change on populations. Additionally, genetic diversity, a prerequisite for adaptive responses, is reduced in Baltic compared to Atlantic populations. On the one hand, adaptive transgenerational plasticity (TGP) might buffer the effects of environmental change, which may be of particular importance under reduced genetic variation. On the other hand, physiological trade-offs due to environmental stress may hamper parental provisioning to offspring thereby intensifying the impact of climate change across generations (nonadaptive TGP). Here, we studied both hypothesis of adaptive and nonadaptive TGP in the three-spined stickleback (Gasterosteus aculeatus) fish model along the strong salinity gradient of the Baltic Sea in a space-for-time experiment. Each population tolerated desalination well, which was not altered by parental exposure to low salinity. Despite a common marine ancestor, populations locally adapted to low salinity lost their ability to cope with fully marine conditions, resulting in lower survival and reduced relative fitness. Negative transgenerational effects were evident in early life stages, but disappeared after selection via mortality occurred during the first 12-30 days posthatch. Modeling various strengths of selection, we showed that nonadaptive transgenerational plasticity accelerated evolution by increasing directional selection within the offspring generation. Qualitatively, when genetic diversity is large, we predict that such effects will facilitate rapid adaptation and population persistence, while below a certain threshold populations suffer a higher risk of local extinction. Overall, our results suggest that transgenerational plasticity and selection are not independent of each other and thereby highlight a current gap in TGP studies.

Hook, Line and Infection: A Guide to Culturing Parasites, Establishing Infections and Assessing Immune Responses in the Three-Spined Stickleback.

The three-spined stickleback (Gasterosteus aculeatus) is a model organism with an extremely well-characterized ecology, evolutionary history, behavioural repertoire and parasitology that is coupled with published genomic data. These small temperate zone fish therefore provide an ideal experimental system to study common diseases of coldwater fish, including those of aquacultural importance. However, detailed information on the culture of stickleback parasites, the establishment and maintenance of infections and the quantification of host responses is scattered between primary and grey literature resources, some of which is not readily accessible. Our aim is to lay out a framework of techniques based on our experience to inform new and established laboratories about culture techniques and recent advances in the field. Here, essential knowledge on the biology, capture and laboratory maintenance of sticklebacks, and their commonly studied parasites is drawn together, highlighting recent advances in our understanding of the associated immune responses. In compiling this guide on the maintenance of sticklebacks and a range of common, taxonomically diverse parasites in the laboratory, we aim to engage a broader interdisciplinary community to consider this highly tractable model when addressing pressing questions in evolution, infection and aquaculture.

Animal Navigation: The Eel's Magnetic Guide to the Gulf Stream.

The geographic distribution of migratory species can span thousands of kilometers. Yet, traits that enable large-scale migrations are poorly understood. A recent study demonstrates that juvenile eels use the Earth's magnetism for their dispersal, with possible implications for their evolution.

Experimental evidence that parasites drive eco-evolutionary feedbacks.

Host resistance to parasites is a rapidly evolving trait that can influence how hosts modify ecosystems. Eco-evolutionary feedbacks may develop if the ecosystem effects of host resistance influence selection on subsequent host generations. In a mesocosm experiment, using a recently diverged (<100 generations) pair of lake and stream three-spined sticklebacks, we tested how experimental exposure to a common fish parasite (Gyrodactylus spp.) affects interactions between hosts and their ecosystems in two environmental conditions (low and high nutrients). In both environments, we found that stream sticklebacks were more resistant to Gyrodactylus and had different gene expression profiles than lake sticklebacks. This differential infection led to contrasting effects of sticklebacks on a broad range of ecosystem properties, including zooplankton community structure and nutrient cycling. These ecosystem modifications affected the survival, body condition, and gene expression profiles of a subsequent fish generation. In particular, lake juvenile fish suffered increased mortality in ecosystems previously modified by lake adults, whereas stream fish showed decreased body condition in stream fish-modified ecosystems. Parasites reinforced selection against lake juveniles in lake fish-modified ecosystems, but only under oligotrophic conditions. Overall, our results highlight the overlapping timescales and the interplay of host-parasite and host-ecosystem interactions. We provide experimental evidence that parasites influence host-mediated effects on ecosystems and, thereby, change the likelihood and strength of eco-evolutionary feedbacks.

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

BACKGROUND: The Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates and consists of the most polymorphic genes known to date. Due to this complexity, however, MHC remains to be characterized in many species including any Neotropical cichlid fish. Neotropical crater lake cichlids are ideal models to study evolutionary processes as they display one of the most convincing examples of sympatric and repeated parallel radiation events within and among isolated crater lakes. RESULTS: Here, we characterized the genes of MHC class IIB chain of the Midas cichlid species complex (Amphilophus cf. citrinellus) including fish from five lakes in Nicaragua. We designed 19 new specific primers anchored in a stepwise fashion in order to detect all alleles present. We obtained 866 genomic DNA (gDNA) sequences from thirteen individuals and 756 additional sequences from complementary DNA (cDNA) of seven of those individuals. We identified 69 distinct alleles with up to 25 alleles per individual. We also found considerable intron length variation and mismatches of alleles detected in cDNA and gDNA suggesting that some loci have undergone pseudogenization. Lastly, we created a model of protein structure homology for each allele and identified their key structural components. CONCLUSIONS: Overall, the Midas cichlid has one of the most diverse repertoires of MHC class IIB genes known, which could serve as a powerful tool to elucidate the process of divergent radiations, colonization and speciation in sympatry.

Mate choice in sticklebacks reveals that immunogenes can drive ecological speciation.

Adaptation to ecologically contrasting niches can lead to the formation of new species. Theoretically, this process of ecological speciation can be driven by pleiotropic "magic traits" that genetically link natural and sexual selection. To qualify as a true magic trait, the pleiotropic function of a gene must be reflected in biologically relevant mechanisms underlying both local adaptation and mate choice. The immune genes of the major histocompatibility complex (MHC) contribute to parasite resistance and also play a major role in sexual selection. Hence, the MHC may encode a candidate magic trait. Using diverging 3-spined stickleback populations from a connected lake-river habitat, we show with mate choice experiments in a flow channel that polymorphic MHC genes probably underlie assortative mating with respect to particular habitat-adapted ecotypes, potentially resulting in reproductive isolation. By manipulating olfactory cues in controlled experiments, we show that female sticklebacks employ MHC-dependent male olfactory signals to select mates with which they can achieve a habitat-specific MHC gene structure that optimally protects their offspring against local parasites. By using MHC-based olfactory signals, females thus select individuals of their own population as mates. Our results demonstrate how mate choice and parasite resistance may be functionally linked. These findings suggest that MHC genes are pleiotropic and encode a true magic trait of biologically significant effect.