Transcriptomic responses of Atlantic salmon (Salmo salar) to environmental enrichment during juvenile rearing.

Captive rearing programs (hatcheries) are often used in conservation and management efforts for at-risk salmonid fish populations. However, hatcheries typically rear juveniles in environments that contrast starkly with natural conditions, which may lead to phenotypic and/or genetic changes that adversely affect the performance of juveniles upon their release to the wild. Environmental enrichment has been proposed as a mechanism to improve the efficacy of population restoration efforts from captive-rearing programs; in this study, we examine the influence of environmental enrichment during embryo and yolk-sac larval rearing on the transcriptome of Atlantic salmon (Salmo salar). Full siblings were reared in either a hatchery environment devoid of structure or an environment enriched with gravel substrate. At the end of endogenous feeding by juveniles, we examined patterns of gene transcript abundance in head tissues using the cGRASP-designed Agilent 4×44K microarray. Significance analysis of microarrays (SAM) indicated that 808 genes were differentially transcribed between the rearing environments and a total of 184 gene ontological (GO) terms were over- or under-represented in this gene list, several associated with mitosis/cell cycle and muscle and heart development. There were also pronounced differences among families in the degree of transcriptional response to rearing environment enrichment, suggesting that gene-by-environment effects, possibly related to parental origin, could influence the efficacy of enrichment interventions.

Phenotype-environment association of the oxygen transport system in trimorphic European whitefish (Coregonus lavaretus) populations.

Replicated adaptive radiation events, typified by phenotypic divergence across resource axes, provide important insight into the eco-evolutionary dynamics that lead to the formation of new species. Here, we show that in trimorphic adaptive radiations of European whitefish (Coregonus lavaretus), divergence of the oxygen transport system has occurred across the pelagic/littoral (shallow)-profundal (deep) resource axis, and at multiple biological scales. Profundal whitefish exhibited significantly larger red blood cells (RBCs), a greater proportion of cathodic hemoglobin protein components, and higher hemoglobin transcript abundance in kidney compared to littoral and pelagic morphs. Hemoglobin transcript abundance in brain and gill, but not kidney, and anodic hemoglobin protein component diversity in blood were also linked to variation at an intronic single nucleotide polymorphism (SNP). As the whitefish morphs differ in population genetic structure at this SNP, hemoglobin transcript and protein divergence between profundal and pelagic/littoral morphs is likely being driven by genetic divergence. Our findings, along with our previous work on lake whitefish, highlight the importance of the oxygen transport system to the postglacial colonization of novel lacustrine environments by whitefish throughout the northern hemisphere.

Variable extent of parallelism in respiratory, circulatory, and neurological traits across lake whitefish species pairs.

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.

Parallelism in the oxygen transport system of the lake whitefish: the role of physiological divergence in ecological speciation.

In North America, populations of lake whitefish (Coregonus clupeaformis) have evolved sympatric 'dwarf' and 'normal' ecotypes that are associated with distinct trophic niches within lakes. Trophic specialization should place diverging physiological demands on individuals, and thus, genes and phenotypes associated with energy production represent ideal candidates for studies of adaptation. Here, we test for the parallel divergence of traits involved in oxygen transport in dwarf and normal lake whitefish from Québec, Canada and Maine, USA. We observed significant differences in red blood cell morphology between the ecotypes. Specifically, dwarfs exhibited larger nuclei and a higher nucleus area/total cell area than normal whitefish in all of the lakes examined. In addition, isoelectric focusing gels revealed variation in the haemoglobin protein components found in whitefish. Dwarf and normal whitefish exhibited a similar number of protein components, but the composition of these components differed, with dwarf whitefish bearing a greater proportion of cathodic components compared to the normals. Furthermore, dwarf whitefish showed significant haemoglobin gene upregulation in the brain compared with the levels shown in normals. Together, our results indicate that metabolic traits involved in oxygen transport differ between the whitefish ecotypes and the strong parallel patterns of divergence observed across lakes implicates ecologically driven selection pressures. We discuss the function of these traits in relation to the differing trophic niches occupied by the whitefish and the potential contributions of trait plasticity and genetic divergence to energetic adaptation.

Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar).

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 0+ and 1+, and 1+ and 2+ 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 MHC-dependent 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.

Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha).

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.