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Females choose specific mates in order to produce fitter offspring. However, several factors interfere with females’control over fertilization of their eggs, including sneaker males and phenotypically unpredictable allele segregation during meiosis. Mate choice at the individual level thus provides only a poor approximation for obtaining the best genetic match. Consequently, postcopulatory sperm selection by female oocytes has been proposed as a mechanism to achieve complementary combinations of parental haplotypes. Here, using controlled in vitro fertilization of three-spined stickleback eggs, we find haplotype-specific fertilization bias toward gametes with complementary major histocompatibility complex (MHC) immunogenes. The resulting zygote (and thus offspring) genotypes exhibit an intermediate level of individual MHC diversity that was previously shown to confer highest pathogen resistance. Our finding of haplotype-specific gamete selection thus represents an intriguing mechanism for fine-tuned optimization of the offspring’s immune gene composition and an evolutionary advantage in the Red Queen dynamics of host-parasite coevolution.

Anthropogenic stressors, such as pollutants, act as selective factors that can leave measurable changes in allele frequencies in the genome. Metals are of particular concern among pollutants, because of interference with vital biological pathways. We use the three-spined stickleback as a model for adaptation to mercury pollution in natural populations. We collected sticklebacks from 21 locations in Flanders (Belgium), measured the accumulated levels of mercury in the skeletal muscle tissue, and genotyped the fish by sequencing (GBS). The spread of muscle mercury content across locations was considerable, ranging from 21.5 to 327 ng/g dry weight (DW). We then conducted a genome-wide association study (GWAS) between 28,450 single nucleotide polymorphisms (SNPs) and the accumulated levels of mercury, using different approaches. Based on a linear mixed model analysis, the GWAS yielded multiple hits with a single top hit on Chromosome 4, with eight more SNPs suggestive of association. A second approach, a latent factor mixed model analysis, highlighted one single SNP on Chromosome 11. Finally, an outlier test identified one additional SNP on Chromosome 4 that appeared under selection. Out of all ten SNPs we identified as associated with mercury in muscle, three SNPs all located on Chromosome 4 and positioned within a 2.5 kb distance of an annotated gene. Based on these results and the genome coverage of our SNPs, we conclude that the selective effect of mercury pollution in Flanders causes a significant association with at least one locus on Chromosome 4 in three-spined stickleback.

The immunologically important major histocompatibility complex (MHC) harbors some of the most polymorphic genes in vertebrates. These genes presumably evolve under parasite-mediated selection and frequently show inconsistent allelic genealogies, where some alleles are more similar between species than within species. This phenomenon is thought to arise either from convergent evolution under parallel selection or from the preservation of ancient allelic lineages beyond speciation events (trans-species polymorphism, TSP). Here, we examine natural populations of two sympatric stickleback species (Gasterosteus aculeatus and Pungitius pungitius) to investigate the contribution of these two mechanisms to the evolution of inconsistent allelic genealogies at the MHC. Overlapping parasite taxa between the two host species in three different habitats suggest contemporary parallel selection on the MHC genes. Accordingly, we detected a lack of species-specific phylogenetic clustering in the immunologically relevant antigen-binding residues of the MHC IIB genes which contrasted with the rest of the coding and noncoding sequence. However, clustering was not habitat-specific and a codon-usage analysis revealed patterns of similarity by descent. In this light, common descent via TSP, in combination with intraspecies gene conversion, rather than convergent evolution is the more strongly supported scenario for the inconsistent genealogy at the MHC.

Parasite virulence varies greatly. Theory predicts that this arises from parasites optimising a trade‐off between the mortality they inflict on current hosts, and their transmission to future hosts. The effect of the environment on this co‐evolution is rarely considered. Geographic mosaics are fertile systems for studying co‐evolution, but again, the diversity of outcomes is often assumed to result from co‐evolutionary dynamism, rather than being moulded by the environment. Here, we quantify variation in virulence among lakes in a geographic mosaic of co‐evolution between a trematode ectoparasite (Gyrodactylus arcuatus) and its three‐spined stickleback (Gasterosteus aculeatus) host. Virulence varies greatly in this system, and parasites are generally locally adapted to their hosts. Parasites are also locally adapted to the water in their own lake, and virulence is strongly related to lake pH, the dominant axis of abiotic environmental variation in this system. These results suggest that the evolution of virulence can be substantially affected by the abiotic environment, which has important implications for understanding co‐evolution. There are also implications for the evolutionary management of disease, e.g. ectoparasites in aquaculture, the impacts of which might be expected to reduce given ongoing acidification of aquatic ecosystems. A plain language summary is available for this article. Plain Language Summary

The role of microplastics as chemical vectors delivering environmental contaminants into biota has been proposed, but their environmental relevance remains an issue of a debate. In this paper we compared the propensity and relative importance of synthetic polymer microparticles (glassy polystyrene (PS) and rubbery polyethylene (PE)) and silica glass particles (SG) to act as vectors for hydrophobic organic chemicals (HOCs) into fish after ingestion. Particles were spiked with three HOCs (17α-ethinylestradiol, chlorpyrifos and benzo(α)pyrene), which differ in hydrophobicity and induce well-known biomarker responses. Three-spined stickleback were exposed to 8 different diets: control diets (1), diets with non-spiked particles (2-4), diets containing a mixture of particles spiked with 3 model contaminants (5-7) and, finally, diets loaded with only the chemical mixture (8), for 14 days. Chemical sorption onto the particles was quantified and chemical transfer into the fish was investigated via biomarkers (CYP1a, ERα, VTG and AChE) in fish intestine, liver and brain and quantification of HOCs in fish muscle. Results demonstrated particle-mediated chemical transfer of moderately hydrophobic contaminants into fish. While PS and PE particles mediated higher chemical transfer and tissue accumulation of 17α-ethinylestradiol and chlorpyrifos than SG, the overall chemical transfer was found to be very low. The present work suggested that chemical sorption, desorption and subsequent transfer of chemicals in vivo depends on multiple interconnected factors, including physicochemical properties of particles and contaminants, as well as toxicokinetic and toxicodynamic interactions. The biomarker approach was, however, suboptimal for assessing chemical transfer when addressing particle-associated chemical mixtures.

1. There is growing interest in the causes and consequences of animal temperaments. Temperament behaviours often have heritable components, but ecological variables can also affect them. Numerous variables are likely to differ between habitats, and these may interact to influence temperament behaviours. 2. Temperament behaviours may be correlated within populations (behavioural syndromes), although the underlying causes of such correlations are currently unclear. 3. We analysed three different temperament behaviours and learning ability in three-spined sticklebacks, Gasterosteus aculeatus, to determine how different ecological variables influence them both within and between populations. We selected populations from four ponds and four rivers that varied naturally in their exposure to predators. 4. High-predation river populations were significantly less bold than a high-predation pond and low-predation river populations, and low-predation pond populations were significantly less bold than a high-predation pond population. Within populations, temperament behaviours were correlated in one high-predation river population only. 5. These results suggest that multiple ecological factors can interact to affect temperament behaviours between populations, and also correlations in those behaviours within populations.

Theory predicts that staying in a refuge has benefits in terms of predator avoidance and costs in terms of lost feeding opportunities. In this study, we investigated how the relative importance of these costs and benefits changes with increasing body length. This is of particular interest in animals such as fish, which show continuous growth throughout their lives. Our results suggest that larger fish are subject to lower predation risks and are less affected by food deprivation than small fish, with fish decreasing their responses to food-deprivation treatments more strongly with increasing body length than to predation treatments. This may explain our observation that large fish emerged later from a refuge than small ones and spent shorter times outside the refuge. The key role of differential responses to food deprivation was further illustrated by the finding that the relative weight loss of individual fish was strongly correlated with a reduction in hiding time even in the absence of body length differences. The importance of inter-individual differences in metabolic rates for the decision-making behaviour of animals is discussed.

Predator-prey interactions play a key life history role, as animals cope with changing predation risk and opportunities to hunt prey. It has recently been shown that the hunting success of sticklebacks (Gasterosteus aculeatus) targeting fish larvae is dependent on both the size of the prey and the prior exposure of its species to stickleback predation. The purpose of the current study was to identify the behavioural predator-prey interactions explaining the success or failure of sticklebacks hunting larvae of three potential prey species [roach (Rutilus rutilus), perch (Perca fluviatilis) and whitefish (Coregonus wartmannii)] in a 3D environment. Trials were carried out for each prey species at four different size classes in a standardised laboratory setup and were recorded using a slow motion, stereo camera setup. 75 predator-prey interactions including both failed and successful hunts were subject to the analysis. 3D track analysis indicated that sticklebacks applied different strategies. Prey with less complex predator escape responses, i.e. whitefish larvae, were hunted using a direct but stealthy approach ending in a lunge, while the behaviourally more complex roach and perch larvae were hunted with a faster approach. A multivariate logistic regression identified that slow average speed and acceleration of the prey in the initial stages of the hunt increased the probability of stickleback success. Furthermore, predators adjusted their swimming direction more often when hunting larger whitefish compared to smaller whitefish. The results suggest that appropriate and adequately timed avoidance behaviours, which vary between prey species and ontogenetic stages, significantly increase the chances of outmanoeuvring and escaping stickleback predation. Small whitefish larvae can reach similar levels of swimming performance compared to older conspecifics, but display ineffective anti-predator behaviours, resulting in higher hunting success for sticklebacks. Thus, the development of appropriate anti-predator behaviours depending on size appears to be the crucial factor to escaping predation.

Marine stickleback fish have colonized and adapted to thousands of streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high-quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of twenty additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine–freshwater divergence. Our results indicate that reuse of globally shared standing genetic variation, including chromosomal inversions, has an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine–freshwater evolution, but regulatory changes appear to predominate in this well known example of repeated adaptive evolution in nature. A reference genome sequence for threespine sticklebacks, and re-sequencing of 20 additional world-wide populations, reveals loci used repeatedly during vertebrate evolution; multiple chromosome inversions contribute to marine-freshwater divergence, and regulatory variants predominate over coding variants in this classic example of adaptive evolution in natural environments. The genomics of stickleback speciation Threespine sticklebacks have become a powerful model for studying the molecular basis of adaptive evolution. This paper presents a high-quality reference genome sequence, along with genomes of 20 further individuals from a global set of marine and freshwater populations. Genomic analysis reveals that reuse of globally shared standing genetic variation plays an important part in repeated evolution of distinct stickleback populations, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. The data are consistent with an important role for regulatory changes during parallel evolution of marine and freshwater sticklebacks.

Hybrid incompatibilities occur when interactions between opposite ancestry alleles at different loci reduce the fitness of hybrids. Most work on incompatibilities has focused on those that are “intrinsic,” meaning they affect viability and sterility in the laboratory. Theory predicts that ecological selection can also underlie hybrid incompatibilities, but tests of this hypothesis using sequence data are scarce. In this article, we compiled genetic data for F 2 hybrid crosses between divergent populations of threespine stickleback fish ( Gasterosteus aculeatus L.) that were born and raised in either the field (seminatural experimental ponds) or the laboratory (aquaria). Because selection against incompatibilities results in elevated ancestry heterozygosity, we tested the prediction that ancestry heterozygosity will be higher in pond-raised fish compared to those raised in aquaria. We found that ancestry heterozygosity was elevated by approximately 3% in crosses raised in ponds compared to those raised in aquaria. Additional analyses support a phenotypic basis for incompatibility and suggest that environment-specific single-locus heterozygote advantage is not the cause of selection on ancestry heterozygosity. Our study provides evidence that, in stickleback, a coarse—albeit indirect—signal of environment-dependent hybrid incompatibility is reliably detectable and suggests that extrinsic incompatibilities can evolve before intrinsic incompatibilities.