Genetic growth potential, rather than phenotypic size, predicts migration phenotype in Atlantic salmon

Knowledge of the relative importance of genetic versus environmental determinants of major developmental transitions is pertinent to understanding phenotypic evolution. In salmonid fishes, a major developmental transition enables a risky seaward migration that provides access to feed resources. In Atlantic salmon, initiation of the migrant phenotype, and thus age of migrants, is presumably controlled via thresholds of a quantitative liability, approximated by body size expressed long before the migration. However, how well size approximates liability, both genetically and environmentally, remains uncertain. We studied 32 Atlantic salmon families in two temperatures and feeding regimes (fully fed, temporarily restricted) to completion of migration status at age 1 year. We detected a lower migrant probability in the cold (0.42) than the warm environment (0.76), but no effects of male maturation status or feed restriction. By contrast, body length in late summer predicted migrant probability and its control reduced migrant probability heritability by 50-70%. Furthermore, migrant probability and length showed high heritabilities and between-environment genetic correlations, and were phenotypically highly correlated with stronger genetic than environmental contributions. Altogether, quantitative estimates for the genetic and environmental effects predicting the migrant phenotype indicate, for a given temperature, a larger importance of genetic than environmental size effects.Peer reviewe

Genetic variation for upper thermal tolerance diminishes within and between populations with increasing acclimation temperature in Atlantic salmon

Populations may counteract lasting temperature changes or recurrent extremes through plasticity or adaptation. However, it remains underexplored how outbreeding, either naturally, unintentionally, or facilitated, may modify a local response potential and whether genotype-by-environment interactions or between-trait correlations can restrict this potential. We quantified population differences and outbreeding effects, within-population genetic variation, and plasticity of these, for thermal performance proxy traits using 32 pedigreed wild, domesticated, and wild-domesticated Atlantic salmon families reared under common-garden conditions. Following exposure to ambient cold (11.6 °C) or ~4° and ~8° warmer summer temperatures, populations differed notably for body length and critical thermal maximum (CTmax) and for thermal plasticity of length, condition, and CTmax, but not for haematocrit. Line-cross analysis suggested mostly additive and some dominant outbreeding effects on means and solely additive outbreeding effects on plasticity. Heritability was detected for all traits. However, with increasing acclimation temperature, differences in CTmax between populations and CTmax heritability diminished, and CTmax breeding values re-ranked. Furthermore, CTmax and body size were negatively correlated at the genetic and phenotypic levels, and there was indirect evidence for a positive correlation between growth potential and thermal performance breadth for growth. Thus, population differences (including those between wild and domesticated populations) in thermal performance and plasticity may present a genetic resource in addition to the within-population genetic variance to facilitate, or impede, thermal adaptation. However, unfavourable genotype-by-environment interactions and negative between-trait correlations may generally hamper joint evolution in response to an increase in average temperature and temporary extremes.publishedVersio

Transcription Profiles of Age-at-Maturity-Associated Genes Suggest Cell Fate Commitment Regulation as a Key Factor in the Atlantic Salmon Maturation Process

Despite recent taxonomic diversification in studies linking genotype with phenotype, follow-up studies aimed at understanding the molecular processes of such genotype-phenotype associations remain rare. The age at which an individual reaches sexual maturity is an important fitness trait in many wild species. However, the molecular mechanisms regulating maturation timing processes remain obscure. A recent genome-wide association study in Atlantic salmon (Salmo salar) identified large-effect age-at-maturity-associated chromosomal regions including genes vgll3, akap11 and six6, which have roles in adipogenesis, spermatogenesis and the hypothalamic-pituitary-gonadal (HPG) axis, respectively. Here, we determine expression patterns of these genes during salmon development and their potential molecular partners and pathways. Using Nanostring transcription profiling technology, we show development- and tissue-specific mRNA expression patterns for vgll3, akap11 and six6. Correlated expression levels of vgll3 and akap11, which have adjacent chromosomal location, suggests they may have shared regulation. Further, vgll3 correlating with arhgap6 and yap1, and akap11 with lats1 and yap1 suggests that Vgll3 and Akap11 take part in actin cytoskeleton regulation. Tissue-specific expression results indicate that vgll3 and akap11 paralogs have sex-dependent expression patterns in gonads. Moreover, six6 correlating with slc38a6 and rtn1, and Hippo signaling genes suggests that Six6 could have a broader role in the HPG neuroendrocrine and cell fate commitment regulation, respectively. We conclude that Vgll3, Akap11 and Six6 may influence Atlantic salmon maturation timing via affecting adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.Peer reviewe

Cytosine methylation patterns suggest a role of methylation in plastic and adaptive responses to temperature in European grayling (Thymallus thymallus) populations

Temperature is a key environmental parameter affecting both the phenotypes and distributions of organisms, particularly ectotherms. Rapid organismal responses to thermal environmental changes have been described for several ectotherms; however, the underlying molecular mechanisms often remain unclear. Here, we studied whole genome cytosine methylation patterns of European grayling (Thymallus thymallus) embryos from five populations with contemporary adaptations of early life history traits at either 'colder' or 'warmer' spawning grounds. We reared fish embryos in a common garden experiment using two temperatures that resembled the 'colder' and 'warmer' conditions of the natal natural environments. Genome-wide methylation patterns were similar in populations originating from colder thermal origin subpopulations, whereas single nucleotide polymorphisms uncovered from the same data identified strong population structure among isolated populations, but limited structure among interconnected populations. This was surprising because the previously studied gene expression response among populations was mostly plastic, and mainly influenced by the developmental temperature. These findings support the hypothesis of the magnified role of epigenetic mechanisms in modulating plasticity. The abundance of consistently changing methylation loci between two warmer-to-colder thermal origin population pairs suggests that local adaptation has shaped the observed methylation patterns. The dynamic nature of the methylomes was further highlighted by genome-wide and site-specific plastic responses. Our findings support both the presence of a plastic response in a subset of CpG loci, and the evolutionary role of methylation divergence between populations adapting to contrasting thermal environments.Peer reviewe

The strength and form of natural selection on transcript abundance in the wild

Gene transcription variation is known to contribute to disease susceptibility and adaptation, but we currently know very little about how contemporary natural selection shapes transcript abundance. Here, we propose a novel analytical framework to quantify the strength and form of ongoing natural selection at the transcriptome level in a wild vertebrate. We estimated selection on transcript abundance in a cohort of a wild salmonid fish (Salmo trutta) affected by an extracellular myxozoan parasite (Tetracapsuloides bryosalmonae) through mark-recapture field sampling and the integration of RNA-sequencing with classical regression-based selection analysis. We show, based on fin transcriptomes of the host, that infection by the parasite and subsequent host survival is linked to upregulation of mitotic cell cycle process. We also detect a widespread signal of disruptive selection on transcripts linked to host immune defence, host-pathogen interactions, cellular repair and maintenance. Our results provide insights into how selection can be measured at the transcriptome level to dissect the molecular mechanisms of contemporary evolution driven by climate change and emerging anthropogenic threats. We anticipate that the approach described here will enable critical information on the molecular processes and targets of natural selection to be obtained in real time

Striking Phenotypic Variation yet Low Genetic Differentiation in Sympatric Lake Trout (Salvelinus namaycush)

The study of population differentiation in the context of ecological speciation is commonly assessed using populations with obvious discreteness. Fewer studies have examined diversifying populations with occasional adaptive variation and minor reproductive isolation, so factors impeding or facilitating the progress of early stage differentiation are less understood. We detected non-random genetic structuring in lake trout (Salvelinus namaycush) inhabiting a large, pristine, postglacial lake (Mistassini Lake, Canada), with up to five discernible genetic clusters having distinctions in body shape, size, colouration and head shape. However, genetic differentiation was low (FST = 0.017) and genetic clustering was largely incongruent between several population- and individual-based clustering approaches. Genotype- and phenotype-environment associations with spatial habitat, depth and fish community structure (competitors and prey) were either inconsistent or weak. Striking morphological variation was often more continuous within than among defined genetic clusters. Low genetic differentiation was a consequence of relatively high contemporary gene flow despite large effective population sizes, not migration-drift disequilibrium. Our results suggest a highly plastic propensity for occupying multiple habitat niches in lake trout and a low cost of morphological plasticity, which may constrain the speed and extent of adaptive divergence. We discuss how factors relating to niche conservatism in this species may also influence how plasticity affects adaptive divergence, even where ample ecological opportunity apparently exists

Striking Phenotypic Variation yet Low Genetic Differentiation in Sympatric Lake Trout (Salvelinus namaycush)

The study of population differentiation in the context of ecological speciation is commonly assessed using populations with obvious discreteness. Fewer studies have examined diversifying populations with occasional adaptive variation and minor reproductive isolation, so factors impeding or facilitating the progress of early stage differentiation are less understood. We detected non-random genetic structuring in lake trout (Salvelinus namaycush) inhabiting a large, pristine, postglacial lake (Mistassini Lake, Canada), with up to five discernible genetic clusters having distinctions in body shape, size, colouration and head shape. However, genetic differentiation was low (FST = 0.017) and genetic clustering was largely incongruent between several population- and individual-based clustering approaches. Genotype- and phenotype-environment associations with spatial habitat, depth and fish community structure (competitors and prey) were either inconsistent or weak. Striking morphological variation was often more continuous within than among defined genetic clusters. Low genetic differentiation was a consequence of relatively high contemporary gene flow despite large effective population sizes, not migration-drift disequilibrium. Our results suggest a highly plastic propensity for occupying multiple habitat niches in lake trout and a low cost of morphological plasticity, which may constrain the speed and extent of adaptive divergence. We discuss how factors relating to niche conservatism in this species may also influence how plasticity affects adaptive divergence, even where ample ecological opportunity apparently exists

Know your enemy - Transcriptome of myxozoan Tetracapsuloides bryosalmonae reveals potential drug targets against proliferative kidney disease in salmonids

The myxozoan Tetracapsuloides bryosalmonae is a widely spread endoparasite that causes proliferative kidney disease (PKD) in salmonid fish. We developed an in silico pipeline to separate transcripts of T. bryosalmonae from the kidney tissue of its natural vertebrate host, brown trout (Salmo trutta). After stringent filtering, we constructed a partial transcriptome assembly T. bryosalmonae, comprising 3427 transcripts. Based on homology-restricted searches of the assembled parasite transcriptome and Atlantic salmon (Salmo salar) proteome, we identified four protein targets (Endoglycoceramidase, Legumain-like protease, Carbonic anhydrase 2, Pancreatic lipase-related protein 2) for the development of anti-parasitic drugs against T. bryosalmonae. Earlier work of these proteins on parasitic protists and helminths suggests that the identified anti-parasitic drug targets represent promising chemotherapeutic candidates also against T. bryosalmonae, and strengthen the view that the known inhibitors can be effective in evolutionarily distant organisms. In addition, we identified differentially expressed T. bryosalmonae genes between moderately and severely infected fish, indicating an increased abundance of T. bryosalmonae sporogonic stages in fish with low parasite load. In conclusion, this study paves the way for future genomic research in T. bryosalmonae and represents an important step towards the development of effective drugs against PKD.</p

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar)

Peer reviewe

The strength and form of natural selection on transcript abundance in the wild

Gene transcription variation is known to contribute to disease susceptibility and adaptation, but we currently know very little about how contemporary natural selection shapes transcript abundance. Here, we propose a novel analytical framework to quantify the strength and form of ongoing natural selection at the transcriptome level in a wild vertebrate. We estimated selection on transcript abundance in a cohort of a wild salmonid fish (Salmo trutta) affected by an extracellular myxozoan parasite (Tetracapsuloides bryosalmonae) through mark-recapture field sampling and the integration of RNA-sequencing with classical regression-based selection analysis. We show, based on fin transcriptomes of the host, that infection by the parasite and subsequent host survival is linked to upregulation of mitotic cell cycle process. We also detect a widespread signal of disruptive selection on transcripts linked to host immune defence, host-pathogen interactions, cellular repair and maintenance. Our results provide insights into how selection can be measured at the transcriptome level to dissect the molecular mechanisms of contemporary evolution driven by climate change and emerging anthropogenic threats. We anticipate that the approach described here will enable critical information on the molecular processes and targets of natural selection to be obtained in real time