Contrasting responses to selection in class I and class IIα major histocompatibility-linked markers in salmon

Abstract

Comparison of levels and patterns of genetic variation in natural populations either across loci or against neutral expectation can yield insight into locus-specific differences in the strength and direction of evolutionary forces. We used both approaches to test the hypotheses on patterns of selection on major histocompatibility (MH)-linked markers. We performed temporal analyses of class I and class IIa MH-linked markers and eight microsatellite loci in two Atlantic salmon populations in Ireland on two temporal scales: over six decades and 9 years in the rivers Burrishoole and Delphi, respectively. We also compared contemporary Burrishoole and Delphi samples with nearby populations for the same loci. On comparing patterns of temporal and spatial differentiation among classes of loci, the class IIa MH-linked marker was consistently identified as an outlier compared with patterns at the other microsatellite loci or neutral expectation. We found higher levels of temporal and spatial heterogeneity in heterozygosity (but not in allelic richness) for the class IIa MH-linked marker compared with microsatellites. Tests on both within-and among-population differentiation are consistent with directional selection acting on the class IIa-linked marker in both temporal and spatial comparisons, but only in temporal comparisons for the class I-linked marker. Our results indicate a complex pattern of selection on MH-linked markers in natural populations of Atlantic salmon. These findings highlight the importance of considering selection on MH-linked markers when using these markers for management and conservation purposes.

Spatial and temporal patterns of neutral and adaptive genetic variation in the endangered African wild dog (Lycaon pictus)

“…2009; Fraser et al. 2010), indicating that selection can be spatially and temporally variable (Hedrick 2002; Consuegra et al. 2011).…”

“…2007; Evans et al. 2010; Consuegra et al. 2011), it is also possible that selection is stronger at other regions of the MHC such as MHC class I loci, which are involved in recognition of intracellular viruses, rather than extracellular pathogens and parasites recognised by class II loci.…”

“…guppy, Poecilia reticulata, Fraser et al. 2010; salmon, Salmo salar , Consuegra et al. 2011; water vole, Arvicola terrestris , Oliver et al.…”

Balancing selection on MHC class I in wild brown trout Salmo trutta

“…This dinucleotide microsatellite marker has been demonstrated to be tightly linked to the class I locus in Atlantic salmon Salmo salar L. 1758 (Grimholt et al , 2002). It has been successfully employed previously in studies in S. salar (de Eyto et al , 2007; Consuegra et al , 2011) and S. trutta (Coughlan et al , 2006; Hansen et al , 2007; O’Farrell et al , 2012). The pattern of linkage has been discussed in some detail in these publications.…”

Temporal and spatial instability in neutral and adaptive (MHC) genetic variation in marginal salmon populations

“…Atlantic salmon is also particularly suited for MHC studies as it represents the minimal-essential-MHC in fish, with only two unlinked MHC class I and class II genes expressed 38 39 and evidence of balancing selection acting on potential peptide binding residues (PBRs) in class I 39 and in class II loci 26 38 . Previous studies had shown evidence of salmon MHC-disassortative mating 40 , as well as an association between specific MHC alleles and pathogen resistance 41 42 43 and there are microsatellite markers linked to both class I and class II loci that can be used as good proxies for functional variation at these genes 44 45 46 .…”