Despite growing evidence for parasite-mediated selection on the vertebrate major histocompatibility complex (MHC), little is known about variation in the bacterial parasite community within and among host populations or its influence on MHC evolution. In this study, we characterize variation in the parasitic bacterial community associated with Chinook salmon (Oncorhynchus tshawytscha) fry in five populations in British Columbia (BC), Canada across 2 years, and examine whether bacterial infections are a potential source of selection on the MHC. We found an unprecedented diversity of bacteria infecting fry with a total of 55 unique bacteria identified. Bacterial infection rates varied from 9% to 29% among populations and there was a significant isolation by distance relationship in bacterial community phylogenetic similarity across the populations. Spatial variation in the frequency of infections and in the phylogenetic similarity of bacterial communities may result in differential parasite-mediated selection at the MHC across populations. Across all populations, we found evidence of a heterozygote advantage at the MHC class II, which may be a source of balancing selection on this locus. Interestingly, a co-inertia analysis indicated only susceptibility associations between a few of the MHC class I and II alleles and specific bacterial parasites; there was no evidence that any of the alleles provided resistance to the bacteria. Our results reveal a complex bacterial community infecting populations of a fish and underscore the importance of considering the role of multiple pathogens in the evolution of host adaptations.
As natural populations decline, captive breeding and rearing programs have become essential components of conservation efforts. However, captive rearing can cause unintended phenotypic and/or genetic changes that adversely impact on population restoration efforts. Here, we test whether the exposure of captive-reared Atlantic salmon (Salmo salar) to natural river environments (i.e., "wild exposure") during early life can serve as a mitigation technique to improve the survivorship of descendents in the wild. Using genetic pedigree reconstruction, we observed a two-fold increase in the survivorship of offspring of wild-exposed parents compared to the offspring of captive parents. Our results suggest that harnessing the influence of transgenerational effects in captive-rearing programs can improve the outcomes of endangered species restoration efforts.
Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0þ and 1þ, and 1þ and 2þ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHCdependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.
Parallel adaptive radiation events provide a powerful framework for investigations of ecology's contribution to phenotypic diversification. Ecologically driven divergence has been invoked to explain the repeated evolution of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis) species in multiple lakes in eastern North America. Nevertheless, links between most putatively adaptive traits and ecological variation remain poorly defined within and among whitefish species pairs. Here, we examine four species pairs for variation in gill, heart, and brain size; three traits predicted to show strong phenotypic responses to ecological divergence. In each of the species pairs, normals exhibited larger body size standardized gills compared to dwarfs – a pattern that is suggestive of a common ecological driver of gill size divergence. Within lakes, the seasonal hypoxia experienced in the benthic environment is a likely factor leading to the requirement for larger gills in normals. Interestingly, the morphological pathways used to achieve larger gills varied between species pairs from Québec and Maine, which may imply subtle non-parallelism in gill size divergence related to differences in genetic background. There was also a non-significant trend toward larger hearts in dwarfs, the more active species of the two, whereas brain size varied exclusively among the lake populations. Taken together, our results suggest that the diversification of whitefish has been driven by parallel and non-parallel ecological conditions across lakes. Furthermore, the phenotypic response to ecological variation may depend on genetic background of each population.
Understanding the genetic architecture of phenotypic plasticity is required to assess how populations might respond to heterogeneous or changing environments. Although several studies have examined population‐level patterns in environmental heterogeneity and plasticity, few studies have examined individual‐level variation in plasticity. Here, we use the North Carolina II breeding design and translocation experiments between two populations of Chinook salmon to detail the genetic architecture and plasticity of offspring survival and growth. We followed the survival of 50 800 offspring through the larval stage and used parentage analysis to examine survival and growth through freshwater rearing. In one population, we found that additive genetic, nonadditive genetic and maternal effects explained 25%, 34% and 55% of the variance in larvae survival, respectively. In the second population, these effects explained 0%, 24% and 61% of the variance in larvae survival. In contrast, fry survival was regulated primarily by additive genetic effects, which indicates a shift from maternal to genetic effects as development proceeds. Fry growth also showed strong additive genetic effects. Translocations between populations revealed that offspring survival and growth varied between environments, the degree of which differed among families. These results indicate genetic differences among individuals in their degree of plasticity and consequently their ability to respond to environmental variation.
The major histocompatibility complex (MHC) is thought to be under strong selection pressure because of its integral role in pathogen recognition. Consequently, patterns of MHC genetic variation should reflect selection pressures across the landscape. We examined genetic variation and population genetic structure at the MHC class I-A1 and class II-B1 exons in five Chinook salmon (Oncorhynchus tshawytscha) populations from two geographic regions in British Columbia, Canada. We then compared estimates of population structure at the MHC genes with neutral estimates based on microsatellites to examine the potential for local adaptation at the MHC. Chinook salmon are in decline throughout much of their native range and understanding the degree of local adaptation exhibited by the MHC may be important in conservation planning. Comparisons among populations yielded higher G 0 ST estimates for the MHC class I than expected under neutrality based on the microsatellites. In contrast, the MHC class II tended to exhibit lower G 0 ST values than did the microsatellites. These results suggest that across populations unique selection pressures are driving allele frequency differences at the MHC class I but that the MHC class II may be the subject of homogenizing selection. Rates of nonsynonymous versus synonymous substitutions found in codons associated within the MHC class I and II peptide-binding regions provided strong evidence of positive selection. Together, these results support the hypothesis that selection is influencing genetic variation at the MHC, but suggest that selection pressures may vary at the two classes of loci both at the sequence and population levels.
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