Testing for local adaptation in the Gasterosteus–Gyrodactylus host–parasite system

Background: Parasites are often assumed to be locally adapted to their hosts, while a growing body of literature shows this is not a fixed rule. We used the threespine stickleback (Gasterosteus aculeatus) and its host-specific parasitic flatworm Gyrodactylus gasterostei of the Belgian lowland–upland system to test for local adaptation and assess whether findings are consistent over different life stages. Question: Is the Gasterosteus–Gyrodactylus host–parasite model system an example of local adaptation? Hypothesis: Parasites have higher infection success on sympatric than on allopatric host populations. Methods: F1 laboratory-bred stickleback originating from a lowland and upland population were infected with parasites of lowland and upland origin. We monitored parasite numbers per individual for 6 weeks and for two life stages and calculated the effect size of local adaptation. Results: Infection success of parasites was not higher on sympatric than on allopatric host populations. Instead, total worm load differed among sub-adult host populations, but not among adult host populations. This suggests immune competence differs among host populations at a specific life stage, rather than local adaptation of the parasite.status: publishe

Signatures of selection in the three-spined stickleback along a small-scale brackish water - freshwater transition zone

Local adaptation is often obvious when gene flow is impeded, such as observed at large spatial scales and across strong ecological contrasts. However, it becomes less certain at small scales such as between adjacent populations or across weak ecological contrasts, when gene flow is strong. While studies on genomic adaptation tend to focus on the former, less is known about the genomic targets of natural selection in the latter situation. In this study, we investigate genomic adaptation in populations of the three-spined stickleback Gasterosteus aculeatus L. across a small-scale ecological transition with salinities ranging from brackish to fresh. Adaptation to salinity has been repeatedly demonstrated in this species. A genome scan based on 87 microsatellite markers revealed only few signatures of selection, likely owing to the constraints that homogenizing gene flow puts on adaptive divergence. However, the detected loci appear repeatedly as targets of selection in similar studies of genomic adaptation in the three-spined stickleback. We conclude that the signature of genomic selection in the face of strong gene flow is weak, yet detectable. We argue that the range of studies of genomic divergence should be extended to include more systems characterized by limited geographical and ecological isolation, which is often a realistic setting in nature.status: publishe

Testing for local adaptation in the Gasterosteus-Gyrodactylus host-parasite system

Background: Parasites are often assumed to be locally adapted to their hosts, while a growing body of literature shows this is not a fixed rule. We used the threespine stickleback (Gasterosteus aculeatus) and its host-specific parasitic flatworm Gyrodactylus gasterostei of the Belgian lowland-upland system to test for local adaptation and assess whether findings are consistent over different life stages. Question: Is the Gasterosteus-Gyrodactylus host-parasite model system an example of local adaptation? Hypothesis: Parasites have higher infection success on sympatric than on allopatric host populations. Methods: F1 laboratory-bred stickleback originating from a lowland and upland population were infected with parasites of lowland and upland origin. We monitored parasite numbers per individual for 6 weeks and for two life stages and calculated the effect size of local adaptation. Results: Infection success of parasites was not higher on sympatric than on allopatric host populations. Instead, total worm load differed among sub-adult host populations, but not among adult host populations. This suggests immune competence differs among host populations at a specific life stage, rather than local adaptation of the parasite

A gene with major phenotypic effects as a target for selection versus homogenizing gene flow

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three-spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low-plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North-western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for the low morph in freshwater and for the allele for the complete morph in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta-analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection.status: publishe

Data from: Signatures of selection in the three-spined stickleback along a small scale brackish water - freshwater transition zone

Local adaptation is often obvious when gene flow is impeded, such as observed at large spatial scales and across strong ecological contrasts. However, it becomes less certain at small scales such as between adjacent populations or across weak ecological contrasts, when gene flow is strong. While studies on genomic adaptation tend to focus on the former, less is known about the genomic targets of natural selection in the latter situation. In this study, we investigate genomic adaptation in populations of the three-spined stickleback Gasterosteus aculeatus L. across a small-scale ecological transition with salinities ranging from brackish to fresh. Adaptation to salinity has been repeatedly demonstrated in this species. A genome scan based on 87 microsatellite markers revealed only few signatures of selection, likely owing to the constraints that homogenizing gene flow puts on adaptive divergence. However, the detected loci appear repeatedly as targets of selection in similar studies of genomic adaptation in the three-spined stickleback. We conclude that the signature of genomic selection in the face of strong gene flow is weak, yet detectable. We argue that the range of studies of genomic divergence should be extended to include more systems characterized by limited geographical and ecological isolation, which is often a realistic setting in nature

Multilocus genotypes of three-spined stickleback, Belgian-Dutch lowlands

Genotypes for 87 loci in four populations (L01, L02, L12, U01) of three-spined stickleback. The first and second column identify the population and the fish ID, respectively. Subsequent columns contain diploid genotype data (3+3 digits). Missing values are entered as 000000

A gene with major phenotypic effects as a target for selection vs. homogenizing gene flow

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three-spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low-plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North-western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for the low morph in freshwater and for the allele for the complete morph in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta-analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection

Data from: A gene with major phenotypic effects as a target for selection versus homogenizing gene flow

Genes with major phenotypic effects facilitate quantifying the contribution of genetic vs. plastic effects to adaptive divergence. A classical example is Ectodysplasin (Eda), the major gene controlling lateral plate phenotype in three-spined stickleback. Completely plated marine stickleback populations evolved repeatedly towards low-plated freshwater populations, representing a prime example of parallel evolution by natural selection. However, many populations remain polymorphic for lateral plate number. Possible explanations for this polymorphism include relaxation of selection, disruptive selection, or a balance between divergent selection and gene flow. We investigated 15 polymorphic stickleback populations from brackish and freshwater habitats in coastal North-western Europe. At each site, we tracked changes in allele frequency at the Eda gene between subadults in fall, adults in spring, and juveniles in summer. Eda genotypes were also compared for body size and reproductive investment. We observed a fitness advantage for the Eda allele for low-platedness in freshwater, and for the allele for completely-platedness in brackish water. Despite these results, the differentiation at the Eda gene was poorly correlated with habitat characteristics. Neutral population structure was the best predictor of spatial variation in lateral plate number, suggestive of a substantial effect of gene flow. A meta-analysis revealed that the signature of selection at Eda was weak compared to similar studies in stickleback. We conclude that a balance between divergent selection and gene flow can maintain stickleback populations polymorphic for lateral plate number, and that ecologically relevant genes may not always contribute much to local adaptation, even when targeted by selection

Raeymaekers et al-MolEcol-2014 Eda

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Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids

Divergent natural selection acting on ecological traits, which also affect mate choice, is a key element of ecological speciation theory, but has not previously been demonstrated at the molecular gene level to our knowledge. Here we demonstrate parallel evolution in two cichlid genera under strong divergent selection in a gene that affects both. Strong divergent natural selection fixed opsin proteins with different predicted light absorbance properties at opposite ends of an environmental gradient. By expressing them and measuring absorbance, we show that the reciprocal fixation adapts populations to divergent light environments. The divergent evolution of the visual system coincides with divergence in male breeding coloration, consistent with incipient ecological by-product speciation.status: publishe