Anne-Laure Ferchaud

The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three-spine sticklebacks in divergent environments.

Heterogeneous genomic divergence between populations may reflect selection, but should also be seen in conjunction with gene flow and drift, particularly population bottlenecks. Marine and freshwater three‐spine stickleback (Gasterosteus aculeatus) populations often exhibit different lateral armour plate morphs. Moreover, strikingly parallel genomic footprints across different marine–freshwater population pairs are interpreted as parallel evolution and gene reuse. Nevertheless, in some geographic regions like the North Sea and Baltic Sea, different patterns are observed. Freshwater populations in coastal regions are often dominated by marine morphs, suggesting that gene flow overwhelms selection, and genomic parallelism may also be less pronounced. We used RAD sequencing for analysing 28 888 SNPs in two marine and seven freshwater populations in Denmark, Europe. Freshwater populations represented a variety of environments: river populations accessible to gene flow from marine sticklebacks and large and small isolated lakes with and without fish predators. Sticklebacks in an accessible river environment showed minimal morphological and genomewide divergence from marine populations, supporting the hypothesis of gene flow overriding selection. Allele frequency spectra suggested bottlenecks in all freshwater populations, and particularly two small lake populations. However, genomic footprints ascribed to selection could nevertheless be identified. No genomic regions were consistent freshwater–marine outliers, and parallelism was much lower than in other comparable studies. Two genomic regions previously described to be under divergent selection in freshwater and marine populations were outliers between different freshwater populations. We ascribe these patterns to stronger environmental heterogeneity among freshwater populations in our study as compared to most other studies, although the demographic history involving bottlenecks should also be considered in the interpretation of results.

Conservation genomics of natural and managed populations: building a conceptual and practical framework

The boom of massive parallel sequencing (MPS) technology and its applications in conservation of natural and managed populations brings new opportunities and challenges to meet the scientific questions that can be addressed. Genomic conservation offers a wide range of approaches and analytical techniques, with their respective strengths and weaknesses that rely on several implicit assumptions. However, finding the most suitable approaches and analysis regarding our scientific question are often difficult and time‐consuming. To address this gap, a recent workshop entitled ‘ConGen 2015’ was held at Montana University in order to bring together the knowledge accumulated in this field and to provide training in conceptual and practical aspects of data analysis applied to the field of conservation and evolutionary genomics. Here, we summarize the expertise yield by each instructor that has led us to consider the importance of keeping in mind the scientific question from sampling to management practices along with the selection of appropriate genomics tools and bioinformatics challenges.

The effects of Medieval dams on genetic divergence and demographic history in brown trout populations

BackgroundHabitat fragmentation has accelerated within the last century, but may have been ongoing over longer time scales. We analyzed the timing and genetic consequences of fragmentation in two isolated lake-dwelling brown trout populations. They are from the same river system (the Gudenå River, Denmark) and have been isolated from downstream anadromous trout by dams established ca. 600–800 years ago. For reference, we included ten other anadromous populations and two hatchery strains. Based on analysis of 44 microsatellite loci we investigated if the lake populations have been naturally genetically differentiated from anadromous trout for thousands of years, or have diverged recently due to the establishment of dams.ResultsDivergence time estimates were based on 1) Approximate Bayesian Computation and 2) a coalescent-based isolation-with-gene-flow model. Both methods suggested divergence times ca. 600–800 years bp, providing strong evidence for establishment of dams in the Medieval as the factor causing divergence. Bayesian cluster analysis showed influence of stocked trout in several reference populations, but not in the focal lake and anadromous populations. Estimates of effective population size using a linkage disequilibrium method ranged from 244 to > 1,000 in all but one anadromous population, but were lower (153 and 252) in the lake populations.ConclusionsWe show that genetic divergence of lake-dwelling trout in two Danish lakes reflects establishment of water mills and impassable dams ca. 600–800 years ago rather than a natural genetic population structure. Although effective population sizes of the two lake populations are not critically low they may ultimately limit response to selection and thereby future adaptation. Our results demonstrate that populations may have been affected by anthropogenic disturbance over longer time scales than normally assumed.

Do North Atlantic eels show parallel patterns of spatially varying selection

BackgroundThe two North Atlantic eel species, the European and the American eel, represent an ideal system in which to study parallel selection patterns due to their sister species status and the presence of ongoing gene flow. A panel of 80 coding-gene SNPs previously analyzed in American eel was used to genotype European eel individuals (glass eels) from 8 sampling locations across the species distribution. We tested for single-generation signatures of spatially varying selection in European eel by searching for elevated genetic differentiation using FST-based outlier tests and by testing for significant associations between allele frequencies and environmental variables.ResultsWe found signatures of possible selection at a total of 11 coding-gene SNPs. Candidate genes for local selection constituted mainly genes with a major role in metabolism as well as defense genes. Contrary to what has been found for American eel, only 2 SNPs in our study correlated with differences in temperature, which suggests that other explanatory variables may play a role. None of the genes found to be associated with explanatory variables in European eel showed any correlations with environmental factors in the previous study in American eel.ConclusionsThe different signatures of selection between species could be due to distinct selective pressures associated with the much longer larval migration for European eel relative to American eel. The lack of parallel selection in North Atlantic eels could also be due to most phenotypic traits being polygenic, thus reducing the likelihood of selection acting on the same genes in both species.

Congruent signals of population history but radically different patterns of genetic diversity between mitochondrial and nuclear markers in a mountain lizard

Historical factors, current population size, population connectivity and selective processes at linked loci contribute to shaping contemporary patterns of neutral genetic diversity. It is now widely acknowledged that nuclear and mitochondrial markers react differently to current demography as well as to past history, so the use of both types of markers is often advocated to gain insight on both historical and contemporary processes. We used 12 microsatellite loci genotyped in 13 populations of a mountain lizard (Iberolacerta bonnali) to test whether the historical scenario favoured by a previous mitochondrial study was also supported by nuclear markers and thereby evaluated the consequences of postglacial range movements on nuclear diversity. Congruent signals of recent history were revealed by nuclear and mitochondrial markers using an Approximate Bayesian computation approach, but contemporary patterns of mtDNA and nuclear DNA diversity were radically different. Although dispersal in this species is probably highly restricted at all spatial scales, colonization abilities have been historically good, suggesting capability for reestablishment of locally extinct populations except in fully disconnected habitats.

A low-density SNP array for analyzing differential selection in freshwater and marine populations of threespine stickleback (Gasterosteus aculeatus)

BackgroundThe threespine stickleback (Gasterosteus aculeatus) has become an important model species for studying both contemporary and parallel evolution. In particular, differential adaptation to freshwater and marine environments has led to high differentiation between freshwater and marine stickleback populations at the phenotypic trait of lateral plate morphology and the underlying candidate gene Ectodysplacin (EDA). Many studies have focused on this trait and candidate gene, although other genes involved in marine-freshwater adaptation may be equally important. In order to develop a resource for rapid and cost efficient analysis of genetic divergence between freshwater and marine sticklebacks, we generated a low-density SNP (Single Nucleotide Polymorphism) array encompassing markers of chromosome regions under putative directional selection, along with neutral markers for background.ResultsRAD (Restriction site Associated DNA) sequencing of sixty individuals representing two freshwater and one marine population led to the identification of 33,993 SNP markers. Ninety-six of these were chosen for the low-density SNP array, among which 70 represented SNPs under putatively directional selection in freshwater vs. marine environments, whereas 26 SNPs were assumed to be neutral. Annotation of these regions revealed several genes that are candidates for affecting stickleback phenotypic variation, some of which have been observed in previous studies whereas others are new.ConclusionsWe have developed a cost-efficient low-density SNP array that allows for rapid screening of polymorphisms in threespine stickleback. The array provides a valuable tool for analyzing adaptive divergence between freshwater and marine stickleback populations beyond the well-established candidate gene Ectodysplacin (EDA).

Predicting the genetic impact of stocking in Brook Charr (Salvelinus fontinalis) by combining RAD sequencing and modeling of explanatory variables

In fisheries management, intensive stocking programs are commonly used to enhance population abundance and maintain stock productivity. However, such practices are increasingly raising concerns as multiple studies documented adverse genetic and evolutionary impacts of stocking on wild populations. Improvement of stocking management relies on a better understanding of the dynamic of introgressive hybridization between wild and domestic population and on assessment of the genetic state of wild populations after stocking cessation. In Québec, Canada, over five million captive‐reared Brook Charr (Salvelinus fontinalis) are stocked every year to support recreational fishing activities. Here, we investigated how variation in stocking history and environmental variables, including water temperature, pH, and dissolved oxygen, may influence the impact of stocking practices on the genetic integrity of wild Brook Charr populations. We collected DNA samples (n = 862, average of 30 individuals per lake) from 29 lakes that underwent different stocking intensity through time and also collected environmental parameters for each sampled lake. An average of 4,580 high‐quality filtered SNPs was obtained for each population using genotyping by sequencing (GBS), which were then used to quantify the mean domestic membership of each sampled population. An exhaustive process of model selection was conducted to obtain a best‐fitted model that explained 56% of the variance observed in mean domestic genetic membership. The number of years since the mean year of stocking was the best explanatory variable to predict variation in mean domestic genetic membership whereas environmental characteristics had little influence on observed patterns of admixture. Our model predictions also revealed that each sampled wild population could potentially return to a wild genetic state (absence of domestic genetic background) after stocking cessation. Overall, our study provides new insights on factors determining level of introgressive hybridization and suggests that stocking impacts could be reversible with time.

Do genetic drift and accumulation of deleterious mutations preclude adaptation? Empirical investigation using RADseq in a northern lacustrine fish

Understanding genomic signatures of divergent selection underlying long‐term adaptation in populations located in heterogeneous environments is a key goal in evolutionary biology. In this study, we investigated neutral, adaptive and deleterious genetic variation using 7,192 SNPs in 31 Lake Trout (Salvelinus namaycush) populations (n = 673) from Québec, Canada. Average genetic diversity was low, weakly shared among lakes, and positively correlated with lake size, indicating a major role for genetic drift subsequent to lake isolation. Putatively deleterious mutations were on average at lower frequencies than the other SNPs, and their abundance relative to the entire polymorphism in each population was positively correlated with inbreeding, suggesting that the effectiveness of purifying selection was negatively correlated with inbreeding, as predicted from theory. Despite evidence for pronounced genetic drift and inbreeding, several outlier loci were associated with temperature and found in or close to genes with biologically relevant functions notably related to heat stress and immune responses. Outcomes of gene–temperature associations were influenced by the inclusion of the most inbred populations, in which allele frequencies deviated the most from model predictions. This result illustrates challenge in identifying gene–environment associations in cases of high genetic drift and restricted gene flow and suggests limited adaptation in populations experiencing higher inbreeding. We discuss the relevance of these findings for the conservation and management, notably regarding stocking and genetic rescue, of Lake Trout populations and other species inhabiting highly fragmented habitats.

Non‐parallel divergence across freshwater and marine three‐spined stickleback Gasterosteus aculeatus populations

This work investigated whether multiple freshwater populations of three-spined stickleback Gasterosteus aculeatus in different freshwater catchments in the Jutland Peninsula, Denmark, derived from the same marine populations show repeated adaptive responses. A total of 327 G. aculeatus collected at 13 sampling locations were screened for genetic variation using a combination of 70 genes putatively under selection and 26 neutral genes along with a marker linked to the ectodysplasin gene (eda), which is strongly correlated with plate armour morphs in the species. A highly significant genetic differentiation was found that was higher among different freshwater samples than between marine-freshwater samples. Tests for selection between marine and freshwater populations showed a very low degree of parallelism and no single nucleotide polymorphism was detected as outlier in all freshwater-marine pairwise comparisons, including the eda. This suggests that G. aculeatus is not necessarily the prime example of parallel local adaptation suggested in much of the literature and that important exceptions exist (i.e. the Jutland Peninsula). While marine populations in the results described here showed a high phenotype-genotype correlation at eda, a low association was found for most of the freshwater populations. The most extreme case was found in the freshwater Lake Hald where all low-plated phenotypes were either homozygotes for the allele supposed to be associated with completely plated morphs or heterozygotes, but none were homozygotes for the putative low-plated allele. Re-examination of data from seven G. aculeatus studies agrees in showing a high but partial association between phenotype-genotype at eda in G. aculeatus freshwater populations and that mismatches occur everywhere in the European regions studied (higher in some areas, i.e. Denmark). This is independent of the eda marker used.

Disentangling genetic structure for genetic monitoring of complex populations

Genetic monitoring estimates temporal changes in population parameters from molecular marker information. Most populations are complex in structure and change through time by expanding or contracting their geographic range, becoming fragmented or coalescing, or increasing or decreasing density. Traditional approaches to genetic monitoring rely on quantifying temporal shifts of specific population metrics—heterozygosity, numbers of alleles, effective population size—or measures of geographic differentiation such as FST. However, the accuracy and precision of the results can be heavily influenced by the type of genetic marker used and how closely they adhere to analytical assumptions. Care must be taken to ensure that inferences reflect actual population processes rather than changing molecular techniques or incorrect assumptions of an underlying model of population structure. In many species of conservation concern, true population structure is unknown, or structure might shift over time. In these cases, metrics based on inappropriate assumptions of population structure may not provide quality information regarding the monitored population. Thus, we need an inference model that decouples the complex elements that define population structure from estimation of population parameters of interest and reveals, rather than assumes, fine details of population structure. Encompassing a broad range of possible population structures would enable comparable inferences across biological systems, even in the face of range expansion or contraction, fragmentation, or changes in density. Currently, the best candidate is the spatial Λ‐Fleming‐Viot (SLFV) model, a spatially explicit individually based coalescent model that allows independent inference of two of the most important elements of population structure: local population density and local dispersal. We support increased use of the SLFV model for genetic monitoring by highlighting its benefits over traditional approaches. We also discuss necessary future directions for model development to support large genomic datasets informing real‐world management and conservation issues.