Genomic Signatures of Local Adaptation under High Gene Flow in Lumpfish-Implications for Broodstock Provenance Sourcing and Larval Production.

Aquaculture of the lumpfish (Cyclopterus lumpus L.) has become a large, lucrative industry owing to the escalating demand for "cleaner fish" to minimise sea lice infestations in Atlantic salmon mariculture farms. We used over 10K genome-wide single nucleotide polymorphisms (SNPs) to investigate the spatial patterns of genomic variation in the lumpfish along the coast of Norway and across the North Atlantic. Moreover, we applied three genome scans for outliers and two genotype-environment association tests to assess the signatures and patterns of local adaptation under extensive gene flow. With our 'global' sampling regime, we found two major genetic groups of lumpfish, i.e., the western and eastern Atlantic. Regionally in Norway, we found marginal evidence of population structure, where the population genomic analysis revealed a small portion of individuals with a different genetic ancestry. Nevertheless, we found strong support for local adaption under high gene flow in the Norwegian lumpfish and identified over 380 high-confidence environment-associated loci linked to gene sets with a key role in biological processes associated with environmental pressures and embryonic development. Our results bridge population genetic/genomics studies with seascape genomics studies and will facilitate genome-enabled monitoring of the genetic impacts of escapees and allow for genetic-informed broodstock selection and management in Norway.

Phenotypically Selective Genotyping Realizes More Genetic Gains in a Rainbow Trout Breeding Program in the Presence of Genotype-by-Environment Interactions.

Selective genotyping of phenotypically superior animals may lead to bias and less accurate genomic breeding values (GEBV). Performing selective genotyping based on phenotypes measured in the breeding environment (B) is not necessarily a good strategy when the aim of a breeding program is to improve animals' performance in the commercial environment (C). Our simulation study compared different genotyping strategies for selection candidates and for fish in C in a breeding program for rainbow trout in the presence of genotype-by-environment interactions when the program had limited genotyping resources and unregistered pedigrees of individuals. For the reference population, selective genotyping of top and bottom individuals in C based on phenotypes measured in C led to the highest genetic gains, followed by random genotyping and then selective genotyping of top individuals in C. For selection candidates, selective genotyping of top individuals in B based on phenotypes measured in B led to the highest genetic gains, followed by selective genotyping of top and bottom individuals and then random genotyping. Selective genotyping led to bias in predicting GEBV. However, in scenarios that used selective genotyping of top fish in B and random genotyping of fish in C, predictions of GEBV were unbiased, with genetic correlations of 0.2 and 0.5 between traits measured in B and C. Estimates of variance components were sensitive to genotyping strategy, with an overestimation of the variance with selective genotyping of top and bottom fish and an underestimation of the variance with selective genotyping of top fish. Unbiased estimates of variance components were obtained when fish in B and C were genotyped at random. In conclusion, we recommend phenotypic genotyping of top and bottom fish in C and top fish in B for the purpose of selecting breeding animals and random genotyping of individuals in B and C for the purpose of estimating variance components when a genomic breeding program for rainbow trout aims to improve animals' performance in C.

Local adaptation at the transcriptome level in brown trout: evidence from early life history temperature genomic reaction norms.

Local adaptation and its underlying molecular basis has long been a key focus in evolutionary biology. There has recently been increased interest in the evolutionary role of plasticity and the molecular mechanisms underlying local adaptation. Using transcriptome analysis, we assessed differences in gene expression profiles for three brown trout (Salmo trutta) populations, one resident and two anadromous, experiencing different temperature regimes in the wild. The study was based on an F2 generation raised in a common garden setting. A previous study of the F1 generation revealed different reaction norms and significantly higher QST than FST among populations for two early life-history traits. In the present study we investigated if genomic reaction norm patterns were also present at the transcriptome level. Eggs from the three populations were incubated at two temperatures (5 and 8 degrees C) representing conditions encountered in the local environments. Global gene expression for fry at the stage of first feeding was analysed using a 32k cDNA microarray. The results revealed differences in gene expression between populations and temperatures and population × temperature interactions, the latter indicating locally adapted reaction norms. Moreover, the reaction norms paralleled those observed previously at early life-history traits. We identified 90 cDNA clones among the genes with an interaction effect that were differently expressed between the ecologically divergent populations. These included genes involved in immune- and stress response. We observed less plasticity in the resident as compared to the anadromous populations, possibly reflecting that the degree of environmental heterogeneity encountered by individuals throughout their life cycle will select for variable level of phenotypic plasticity at the transcriptome level. Our study demonstrates the usefulness of transcriptome approaches to identify genes with different temperature reaction norms. The responses observed suggest that populations may vary in their susceptibility to climate change.

Identifying footprints of selection in stocked brown trout populations: a spatio-temporal approach.

Studies of interactions between farmed and wild salmonid fishes have suggested reduced fitness of farmed strains in the wild, but evidence for selection at the genic level is lacking. We studied three brown trout populations in Denmark which have been significantly admixed with stocked hatchery trout (19-64%), along with two hatchery strains used for stocking. The wild populations were represented by contemporary samples (2000-2006) and two of them by historical samples (1943-1956). We analysed 61 microsatellite loci, nine of which showed putative functional relationships [expressed sequence tag (EST)-linked or quantitative trait loci]. F(ST)-based outlier tests provided support for diversifying selection at chromosome regions marked by three loci, two anonymous and one EST-linked. Patterns of differentiation suggested that the loci were candidates for being under diversifying hitch-hiking selection in hatchery vs. wild environments. Analysis of hatchery strain admixture proportions showed that in one wild population, two of the loci showed significantly lower admixture proportions than the putatively neutral loci, implying contemporary selection against alleles introduced by hatchery strain trout. In the most strongly admixed population, however, there was no evidence for selection, possibly because of immigration by stocked trout overcoming selection against hatchery-derived alleles or supportive breeding practices allowing hatchery strain trout to escape natural selection. To our knowledge, this is the first study demonstrating footprints of selection in wild salmonid populations subject to spawning intrusion by farmed fish.

Sixty years of anthropogenic pressure: a spatio-temporal genetic analysis of brown trout populations subject to stocking and population declines.

Analyses of historical samples can provide invaluable information on changes to the genetic composition of natural populations resulting from human activities. Here, we analyse 21 microsatellite loci in historical (archived scales from 1927 to 1956) and contemporary samples of brown trout (Salmo trutta) from six neighbouring rivers in Denmark, to compare the genetic structure of wild populations before and after population declines and stocking with nonlocal strains of hatchery trout. We show that all populations have been strongly affected by stocking, with admixture proportions ranging from 14 to 64%. Historical population genetic structure was characterized by isolation by distance and by positive correlations between historical effective population sizes and habitat area within river systems. Contemporary population genetic structure still showed isolation by distance, but also reflected differences among populations in hatchery trout admixture proportions. Despite significant changes to the genetic composition within populations over time, dispersal rates among populations were roughly similar before and after stocking. We also assessed whether population declines or introgression by hatchery strain trout should be the most significant conservation concern in this system. Based on theoretical considerations, we argue that population declines have had limited negative effects for the persistence of adaptive variation, but admixture with hatchery trout may have resulted in reduced local adaptation. Collectively, our study demonstrates the usefulness of analysing historical samples for identifying the most important consequences of human activities on the genetic structure of wild populations.