Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes

Department of Evolutionary Ecology, Max-Planck-Institute for Limnology, August-Thienemann-Strasse 2, 24306 Plön, Germany.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 06/2007; 274(1617):1523-32. DOI: 10.1098/rspb.2007.0210
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Freshwater populations of three-spined sticklebacks (Gasterosteus aculeatus) in northern Germany are found as distinct lake and river ecotypes. Adaptation to habitat-specific parasites might influence immune capabilities of stickleback ecotypes. Here, naive laboratory-bred sticklebacks from lake and river populations were exposed reciprocally to parasite environments in a lake and a river habitat. Sticklebacks exposed to lake conditions were infected with higher numbers of parasite species when compared with the river. River sticklebacks in the lake had higher parasite loads than lake sticklebacks in the same habitat. Respiratory burst, granulocyte counts and lymphocyte proliferation of head kidney leucocytes were increased in river sticklebacks exposed to lake when compared with river conditions. Although river sticklebacks exposed to lake conditions showed elevated activation of their immune system, parasites could not be diminished as effectively as by lake sticklebacks in their native habitat. River sticklebacks seem to have reduced their immune-competence potential due to lower parasite diversity in rivers.

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    • "Parasite infection in this small fish depends on host ecology (e.g. consumption of intermediate hosts), immune genotype (Matthews et al. 2010; Eizaguirre et al. 2012) and cellular immune function (Kurtz et al. 2004, 2006; Scharsack et al. 2007; Bolnick et al. 2015). The role of immune gene expression in this population differentiation is less clear. "
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    ABSTRACT: Geographic variation in parasite communities can drive evolutionary divergence in host immune genes. However, biotic and abiotic environmental variation can also induce plastic differences in immune function among populations. At present, there is little information concerning the relative magnitudes of heritable versus induced immune divergence in natural populations. We examined immune gene expression profiles of threespine stickleback (Gasterosteus aculeatus) from six lakes on Vancouver Island, British Columbia, Parasite community composition differs between lake types (large or small, containing limnetic-or benthic-like stickleback) and between watersheds. We observed corresponding differences in immune gene expression profiles among wild-caught stickleback, using a set of seven immune genes representing distinct branches of the immune system. To evaluate the role of environmental effects on this differentiation, we experimentally transplanted wild-caught fish into cages in their native lake, or into a nearby foreign lake. Transplanted individuals' immune gene expression converged on patterns typical of their destination lake, deviating from their native expression profile. Transplant individuals' source population had a much smaller effect, suggesting relatively weak genetic underpinning of population differences in immunity, as viewed through gene expression. This strong environmental regulation of immune gene expression provides a counterpoint to the large emerging literature documenting microevolution and genetic diversification of immune function. Our findings illustrate the value of studying immunity in natural environmental settings where the immune system has evolved and actively functions. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Molecular Ecology 06/2015; 24(18). DOI:10.1111/mec.13295 · 6.49 Impact Factor
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    • "Limnetic and benthic sticklebacks from the same lake differed in terms of parasite communities (MacColl 2009), and limnetic sticklebacks had fewer MHC alleles per individual than benthic species (Matthews et al. 2010). Lake and river populations of sticklebacks from Northern Germany differed in both their parasite communities and MHC allele variability, and it was shown that river sticklebacks had less parasite species and fewer MHC alleles than lake sticklebacks (Scharsack et al. 2007, Eizaguirre et al. 2010). For these populations, a pleiotropic role of MHC genes was suggested to drive divergence between ecotypes due to parasite-mediated selection and assortative mating based on MHC-related mate choice (Eizaguirre et al. 2009a). "
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    ABSTRACT: Genes that play key roles in host immunity such as the major histocompatibility complex (MHC) in vertebrates are expected to be major targets of selection. It is well known that environmental conditions can have an effect on host–parasite interactions and may thus influence the selection on MHC. We analyzed MHC class IIß variability over 35 years in a population of perch (Perca fluviatilis) from the Baltic Sea that was split into two populations separated from each other. One population was subjected to heating from cooling water of a nuclear power plant and was isolated from the surrounding environment in an artificial lake, while the other population was not subjected to any change in water temperature (control). The isolated population experienced a change of the allelic composition and a decrease in allelic richness of MHC genes compared to the control population. The two most common MHC alleles showed cyclic patterns indicating ongoing parasite–host coevolution in both populations, but the alleles that showed a cyclic behavior differed between the two populations. No such patterns were observed at alleles from nine microsatellite loci, and no genetic differentiation was found between populations. We found no indications for a genetic bottleneck in the isolated population during the 35 years. Additionally, differences in parasitism of the current perch populations suggest that a change of the parasite communities has occurred over the isolation period, although the evidence in form of in-depth knowledge of the change of the parasite community over time is lacking. Our results are consistent with the hypothesis of a selective sweep imposed by a change in the parasite community.
    Ecology and Evolution 02/2015; 5(7). DOI:10.1002/ece3.1426 · 2.32 Impact Factor
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    • "In particular, the freshwater-increased GCNVs included two genes involved in the inflammatory response (APOL2, NLRC5) and two genes that were homologous to MyHC (ENSGACG00000002902, ENSGACG00000002933). A previous study showed parallel divergences between littoral and pelagic phenotype pairs of three-spined stickleback MHC genes, which are key genes in the immune system and would be associated with parasite communities in each habitat [36]. Various types of myosin genes were reported to have appeared during the evolution of teleost fish, and those variations were supposed to have contributed to the adaptation to variable aquatic conditions [33]. "
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    ABSTRACT: Background Understanding the genetic basis of adaptive evolution is one of the major goals in evolutionary biology. Recently, it has been revealed that gene copy number variations (GCNVs) constitute significant proportions of genomic diversities within natural populations. However, it has been unclear whether GCNVs are under positive selection and contribute to adaptive evolution. Parallel evolution refers to adaptive evolution of the same trait in related but independent lineages, and three-spined stickleback (Gasterosteus aculeatus) is a well-known model organism. Through identification of genetic variations under parallel selection, i.e., variations shared among related but independent lineages, evidence of positive selection is obtained. In this study, we investigated whole-genome resequencing data from the marine and freshwater groups of three-spined sticklebacks from diverse areas along the Pacific and Atlantic Ocean coastlines, and searched for GCNVs under parallel selection. Results We identified 24 GCNVs that showed significant differences in the numbers of mapped reads between the two groups, and this number was significantly larger than that expected by chance. The derived group, i.e., freshwater group, was typically characterized by larger gene-copy numbers, which implied that gene duplications or multiplications helped with adaptation to the freshwater environment. Some of the identified GCNVs were those of multigenic family genes, which is consistent with the theory that fatal effects due to copy-number changes of multigenic family genes tend to be less than those of single-copy genes. Conclusion The identification of GCNVs that were likely under parallel selection suggests that contribution of GCNVs should be considered in studies on adaptive evolution. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-735) contains supplementary material, which is available to authorized users.
    BMC Genomics 08/2014; 15(1):735. DOI:10.1186/1471-2164-15-735 · 3.99 Impact Factor
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