Genomic signatures of parasite-driven natural selection in north European Atlantic salmon (Salmo salar)

Abstract

Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult.Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying interpopulation differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.

Comparison of anadromous and landlocked Atlantic salmon genomes reveals signatures of parallel and relaxed selection across the Northern Hemisphere

“…TA B L E 3 Regions with reduced heterozygosity in anadromous salmon. Listing regions showing consistently reduced heterozygosity in anadromous compared to landlocked populations (intersect of our data and the data from Zueva et al (2018)). Table 1 predominantly expressed in brain and gonads (Figures 2b and S4, File S2).…”

“…The x-axis shows the position in the genome, and the y-axis presents the difference in average heterozygosity (dZHp) between the two groups, where regions with low ZHp in landlocked salmon are present above 0 and regions with low ZHp in anadromous salmon are present below 0. Regions with consistently reduced heterozygosity in landlocked salmon that overlapped with any of the 28 selective sweeps are shown as yellow dots, and regions with consistently reduced heterozygosity in anadromous salmon (intersect of our data and data from Zueva et al (2018)) are shown as red dots. The regions highlighted by yellow and red dots are listed in Table 2 (in bold) and Table 3, respectively ,506,524-32,558,150 51,626 unknown, macf1, rft2 3 61,880,141-61,931,499 51,358 4 11,625,820-11,676,588 50,768 spcs3, wdr17, asb5 5 47,905,828-47,964,764 58,936 eif3e, rspo2 7 44,096,893-44,148,649 51,756 ppfia2 8 11,124,829-11,176,404 51,575 asb5, spcs3, wdr17 8 12,454,313-12,553,935 99,622 8 16,940,959-17,026,461 85,502 unknown, g3bp2, ppm1k, uso1, pkd2, abcg2 11 13,759,622-13,812,520 52,898 cadn 11 17,877,623-17,927,732 50,109 sbf2 14 25,660,660-25,712,400 51,740 tgfbr1 17 44,490,402-44,541,187 50,785 spic, bcl2l13, mybpc3 17 44,642,974-44,693,695 50,721 mch2, igf1, parpbp 27 161,241-236,092 74,851 psmd4, unknown, pip5k1a, znf687 Note:: Gene symbols of genes from the reference annotation are shown as obtained from the annotation against Swiss-Prot, where genes lacking a gene symbol are indicated by "unknown".…”

“…In the salmon tissue distribution dataset ( Figure S4), we observed higher expression in immune-related tissues such as spleen and head kidney, suggesting a possible role of this gene in immune defense in salmon. It is possible that different pathogen or parasite exposure in freshwater and seawater has been a driving force for selection on disease resistance (a topic discussed in more detail by Zueva et al (2018)). Not much is known about cdca4, however, the gene encodes a regulator of transcriptional activation involved in cell proliferation (Hayashi et al, 2006) and has been shown to interact with p53 to promote apoptosis upon DNA damage (Hsieh et al, 2002;Pang et al, 2019).…”

“…Genomic windows where max(ZHp A ) < 0 and min(ZHp L ) > 0, where ZHp A and ZHp L are the ZHp values of a given genomic window from anadromous and landlocked populations, respectively, were considered as having reduced heterozygosity in the anadromous salmon. Regions with consistent reduction in heterozygosity in anadromous salmon were defined as regions with reduced ZHp in anadromous salmon in our sequence-based data that overlapped with windows showing reduced ZHp in anadromous salmon from the dataset presented inZueva et al (2018). The same approach was used to identify regions with consistently reduced ZHp in landlocked populations.…”

Combining species distribution models and population genomics underlines the determinants of range limitation in an emerging parasite

“…In geographic areas in which founder effects and/or bottlenecks have led to a heterogeneous spatial distribution of alleles, parasite distribution could be spatially limited because of the presence of specific alleles conferring resistance (Zhang et al 2015, Charbonnel et al 2019). Next‐Generation Sequencing approaches have recently opened new research avenues by giving access to thousands of both non‐coding and coding markers related to host defense at the genome‐wide level (Wenzel et al 2015, Benavides et al 2016, Zueva et al 2018).…”