Association between Chromosome 4 and mercury accumulation in muscle of the three‐spined stickleback (Gasterosteus aculeatus)

Abstract

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.

Contrasting population genetic responses to migration barriers in two native and an invasive freshwater fish

“…Moreover, local selection may have contributed more to population differentiation in native species. For instance, local pollution may be genotoxic, select for tolerant genotypes, cause local bottlenecks, or alter migration patterns (Calboli et al, 2021; Costa, 2021; Díez‐del‐Molino et al, 2018). The variation in IBD patterns may also be attributed to variation in effective population size.…”

Spleen gene expression is associated with mercury content in three-spined stickleback populations

“…An overview of sampling sites, sample collection, sample preparation, sex determination, and measurement of mercury content in muscle tissue and in the sediment is available in Calboli et al (2021). Here, we provide a summary of these methods, and describe additional procedures relevant for our study.…”

“…Flanders has experienced a significant degree of metal pollution from industrial activities since the 19th century, with very local though scattered signatures of mercury contamination in soils and sediments (Tack et al, 2005; Van Steertegem, 2011, Brosens et al, 2015). Accordingly, mercury concentrations in the muscle tissue of stickleback populations are highly variable, ranging from 21.5 to 327 ng/g dry weight (Calboli et al, 2021). Calboli et al (2021) further revealed that Hg accumulation is associated with specific genomic regions, suggesting a genetic basis for adaptation to mercury-polluted environments in three-spined sticklebacks in Flanders.…”

“…Accordingly, mercury concentrations in the muscle tissue of stickleback populations are highly variable, ranging from 21.5 to 327 ng/g dry weight (Calboli et al, 2021). Calboli et al (2021) further revealed that Hg accumulation is associated with specific genomic regions, suggesting a genetic basis for adaptation to mercury-polluted environments in three-spined sticklebacks in Flanders.…”

Human‐induced evolution: Signatures, processes and mechanisms underneath anthropogenic footprints on natural systems

“…High concentrations of chemicals or heavy metals disrupt metabolic pathways and biological functions, and as such, the pressure imposed is direct and directional for increasing tolerance. With that in mind, Calboli et al (2021) performed a genome-wide association study to investigate the genetic basis of mercury tolerance in sticklebacks (Gasterosteus aculeatus) collected along a gradient of polluted environments. Exploring an association between mercury in muscle tissue and genome-wide genomic variants, Calboli et al found localized genomic regions putatively involved in adaptation to mercury-polluted environments.…”