Footprints of Directional Selection in Wild Atlantic Salmon Populations: Evidence for Parasite-Driven Evolution?

Abstract

Mechanisms of host-parasite co-adaptation have long been of interest in evolutionary biology; however, determining the genetic basis of parasite resistance has been challenging. Current advances in genome technologies provide new opportunities for obtaining a genome-scale view of the action of parasite-driven natural selection in wild populations and thus facilitate the search for specific genomic regions underlying inter-population differences in pathogen response. European populations of Atlantic salmon (Salmo salar L.) exhibit natural variance in susceptibility levels to the ectoparasite Gyrodactylus salaris Malmberg 1957, ranging from resistance to extreme susceptibility, and are therefore a good model for studying the evolution of virulence and resistance. However, distinguishing the molecular signatures of genetic drift and environment-associated selection in small populations such as land-locked Atlantic salmon populations presents a challenge, specifically in the search for pathogen-driven selection. We used a novel genome-scan analysis approach that enabled us to i) identify signals of selection in salmon populations affected by varying levels of genetic drift and ii) separate potentially selected loci into the categories of pathogen (G. salaris)-driven selection and selection acting upon other environmental characteristics. A total of 4631 single nucleotide polymorphisms (SNPs) were screened in Atlantic salmon from 12 different northern European populations. We identified three genomic regions potentially affected by parasite-driven selection, as well as three regions presumably affected by salinity-driven directional selection. Functional annotation of candidate SNPs is consistent with the role of the detected genomic regions in immune defence and, implicitly, in osmoregulation. These results provide new insights into the genetic basis of pathogen susceptibility in Atlantic salmon and will enable future searches for the specific genes involved.

Population genomic analyses of early‐phase Atlantic Salmon (Salmo salar) domestication/captive breeding

“…; Zueva et al. ). Experimental evolution, or ‘evolve and sequence’, studies in D. melanogaster suggest that temperature or parasite treatments may induce major allele frequency shifts at hundreds of loci after only a few generations (Orozco‐terWengel et al.…”

On the maintenance of genetic variation and adaptation to environmental change: considerations from population genomics in fishes

“…References to less recent studies can be found in several review papers (Hemmer‐Hansen et al , ; Pujolar et al , , ; Ulrik et al , ; Willette et al , ; Gaither et al , ; Guo et al , ; Elmer, ; Picq et al , , as well as references in the next section as examples of the most recent studies). In contrast, fewer fish studies have used a landscape genomic framework to detecting selection by finding statistical associations between local allele frequencies and environmental variables and those have mainly been performed on salmonids (Zueva et al , ; Hecht et al , ; Hand et al , ). For instance, Hecht et al () used RADseq to genotype nearly 2000 Chinook salmon Oncorhynchus tshawytscha (Walbaum 1792) from 46 localities at about 20 000 SNPs in order to document environmental adaptation throughout the North American range of the species, from California to Alaska.…”

Signals of heterogeneous selection at an MHC locus in geographically proximate ecotypes of sockeye salmon

“…; Zueva et al . ). Additionally, salmon express a single copy of the MHC class I and MHC class II, simplifying analysis compared with other species that have many copies (Lukacs et al .…”