Translocations are carried out either unintentionally or intentionally for conservation or management reasons. In both cases, translocated populations may genetically impact natural populations via introgression. Understanding how genetic background may affect an establishment in a novel environment and the potential risks for native populations is important for biodiversity conservation. Here, using a panel of 96 SNPs, we monitor the establishment of two genetically and ecologically distinct brown trout populations released into a mountain lake system in central Sweden where trout did not occur prior to the release. The release was carried out in 1979, and we monitor the establishment over the first three decades (5–6 generations) in seven lakes downstream of the release site. We find that extensive hybridization has occurred, and genes from both populations exist in all lakes examined. Genes from the population that was nonmigratory in its native environment have remained to a higher degree in the area close to the release site, while genes from the population that was more migratory in its native habitat have spread further downstream. All established populations exhibit higher levels of genetic diversity than the released populations. Natural, stream-resident brown trout populations occur ~15 km downstream of the release site and below a waterfall that acts as an upstream migration barrier. Released fish have spread genes to these populations but with low introgression rates of 3%–8%. Recently adopted indicators for monitoring genetic diversity were partly able to detect this introgression, emphasizing the usefulness of genetic indicators in management. The SNP panel used in this study provides a similar picture as previously used allozymes, showing that older marker systems with fewer loci may still be useful for describing the population structure.

Genetic diversity is fundamental to the adaptive potential and survival of species. Although its importance has long been recognized in science, it has a history of neglect within policy, until now. The new Global Biodiversity Framework recently adopted by the Convention on Biological Diversity, states that genetic diversity must be maintained at levels assuring adaptive potential of populations, and includes metrics for systematic monitoring of genetic diversity in so called indicators. Similarly, indicators for genetic diversity are being developed at national levels. Here, we apply new indicators for Swedish national use to one of the northernmost salmonid fishes, the Arctic charr (Salvelinus alpinus). We sequence whole genomes to monitor genetic diversity over four decades in three landlocked populations inhabiting protected alpine lakes in central Sweden. We find levels of genetic diversity, inbreeding and load to differ among lakes but remain stable over time. Effective population sizes are generally small (< 500), suggesting a limited ability to maintain adaptive variability if genetic exchange with nearby populations became eliminated. We identify genomic regions potentially shaped by selection; SNPs exhibiting population divergence exceeding expectations under drift and a putative selective sweep acting within one lake to which the competitive brown trout (Salmo trutta) was introduced during the sampling period. Identified genes appear involved in immunity and salinity tolerance. Present results suggest that genetically vulnerable populations of Arctic charr have maintained neutral and putatively adaptive genetic diversity despite small effective sizes, attesting the importance of continued protection and assurance of gene flow among populations.

International policy recently adopted commitments to maintain genetic diversity in wild populations to secure their adaptive potential, including metrics to monitor temporal trends in genetic diversity – so-called indicators. A national programme for assessing trends in genetic diversity was recently initiated in Sweden. Relating to this effort, we systematically assess contemporary genome-wide temporal trends (40 years) in wild populations using the newly adopted indicators and whole genome sequencing (WGS). We use pooled and individual WGS data from brown trout (Salmo trutta) in eight alpine lakes in protected areas. Observed temporal trends in diversity metrics (nucleotide diversity, Watterson's ϴ and heterozygosity) lie within proposed acceptable threshold values for six of the lakes, but with consistently low values in lakes above the tree line and declines observed in these northern-most lakes. Local effective population size is low in all lakes, highlighting the importance of continued protection of interconnected systems to allow genetic connectivity for long-term viability of these populations. Inbreeding (F_ROH) spans 10%–30% and is mostly represented by ancient (<1 Mb) runs of homozygosity, with observations of little change in mutational load. We also investigate adaptive dynamics over evolutionarily short time frames (a few generations); identifying putative parallel selection across all lakes within a gene pertaining to skin pigmentation as well as candidates of selection unique to specific lakes and lake systems involved in reproduction and immunity. We demonstrate the utility of WGS for systematic monitoring of natural populations, a priority concern if genetic diversity is to be protected.

Population extinction is ubiquitous in all taxa. Such extirpations can reduce intraspecific diversity, but the extent to which genetic diversity of surviving populations are affected remains largely unclear. A key concept in this context is the effective population size (N_e), which quantifies the rate at which genetic diversity within populations is lost. N_e was developed for single, isolated populations while many natural populations are instead connected to other populations via gene flow. Recent analytical approaches and software permit modelling of N_e of interconnected populations (metapopulations). Here, we apply such tools to investigate how extinction of subpopulations affects N_e of the metapopulation (N_eMeta) and of separate surviving subpopulations (N_eRx) under different rates and patterns of genetic exchange between subpopulations. We assess extinction effects before and at migration-drift equilibrium. We find that the effect of extinction on N_eMeta increases with reduced connectivity, suggesting that stepping stone models of migration are more impacted than island-migration models when the same number of subpopulations are lost. Furthermore, in stepping stone models, after extinction and before a new equilibrium has been reached, N_eRx can vary drastically among surviving subpopulations and depends on their initial spatial position relative to extinct ones. Our results demonstrate that extinctions can have far more complex effects on the retention of intraspecific diversity than typically recognized. Metapopulation dynamics need heightened consideration in sustainable management and conservation, e.g., in monitoring genetic diversity, and are relevant to a wide range of species in the ongoing extinction crisis. 

Ungulate species have experienced severe declines over the past centuries through overharvesting and habitat loss. Even if many game species have recovered thanks to strict hunting regulation, the genome-wide impacts of overharvesting are still unclear. Here, we examine the temporal and geographical differences in genome-wide diversity in moose (Alces alces) over its whole range in Sweden by sequencing 87 modern and historical genomes. We found limited impact of the 1900s near-extinction event but local variation in inbreeding and load in modern populations, as well as suggestion of a risk of future reduction in genetic diversity and gene flow. Furthermore, we found candidate genes for local adaptation, and rapid temporal allele frequency shifts involving coding genes since the 1980s, possibly due to selective harvesting. Our results highlight that genomic changes potentially impacting fitness can occur over short time scales and underline the need to track both deleterious and selectively advantageous genomic variation.

Population translocations occur for a variety of reasons, from displacement due to climate change to human-induced transfers. Such actions have adverse effects on genetic variation and understanding their microevolutionary consequences requires monitoring. Here, we return to an experimental release of brown trout (Salmo trutta) in order to monitor the genomic effects of population translocations. In 1979, fish from each of two genetically (F_ST = 0.16) and ecologically separate populations were simultaneously released, at one point in time, to a lake system previously void of brown trout. Here, whole-genome sequencing of pooled DNA (Pool-seq) is used to characterize diversity within and divergence between the introduced populations and fish inhabiting two lakes downstream of the release sites, sampled 30 years later (c. 5 generations). Present results suggest that while extensive hybridization has occurred, the two introduced populations are unequally represented in the lakes downstream of the release sites. One population, which is ecologically resident in its original habitat, mainly contributes to the lake closest to the release site. The other population, migratory in its natal habitat, is genetically more represented in the lake further downstream. Genomic regions putatively under directional selection in the new habitat are identified, where allele frequencies in both established populations are more similar to the introduced population stemming from a resident population than the migratory one. Results suggest that the microevolutionary consequences of population translocations, for example, hybridization and adaptation, can be rapid and that Pool-seq can be used as an initial tool to monitor genome-wide effects.

Genetic diversity is the foundation of all biological variation. An approach for sustainable use and protection of genetic diversity is continuous sampling over space and time, i.e. monitoring. It is important to consider genetic changes over contemporary time frames, since most human perturbations have occurred within the last century. Modern molecular tools now enable genome-wide diversity monitoring, also in non-model species.

The work included in this thesis utilizes theoretical and molecular tools to monitor genomic diversity over microevolutionary time frames using salmonid fishes as models. First, the capacity for substructured populations to retain genetic variation following population extinctions was theoretically assessed. Models of effective population size (N_e) relevant to salmonids were used. Further, spatio-temporal genetic patterns of the highly substructured brown trout (Salmo trutta) were empirically estimated. Wild populations were studied using whole-genome sequencing, primarily of pools of individuals (Pool-seq). The brown trout is characterized by a large and complex genome, and genomic resources have, until recently, been lacking. One central aim of this thesis was therefore to evaluate the benefit of using Pool-seq data for monitoring genetic diversity in this species. To this end, disparate natural populations were studied that are, in part, previously described using classic genetic markers. First, I hypothesized that a Pool-seq-only approach developed for non-model species that lack reference genomes could be used to detect population differentiation between two scenarios of coexisting populations. In a second step, two different cases of populations in the wild – one experimental release and one case of protected populations – were monitored over nearly four decades (5-6 brown trout generations) using Pool-seq data. I asked what the levels of diversity and divergence among populations are, whether changes could be detected over contemporary time and if they could be attributed to adaptation.

Paper I demonstrates that the effect of extinction on the rate of diversity change in population systems is more complex than previously recognized. Diversity loss is most prominent when migration within the population system is limited, which suggests that highly substructured population systems, e.g., many salmonids, are particularly vulnerable to population extinction. The utility of Pool-seq for monitoring brown trout populations over contemporary time is demonstrated for the three different cases of brown trout populations (Papers II-IV). Paper II confirms the ability of a Pool-seq-only approach to detect subtle population differentiation. Paper III identifies genome-wide levels of hybridization between populations introduced to a new environment and signs of adaptation in genes putatively involved in metabolism. Paper IV detects significant allele frequency shifts over a limited number of generations. Potentially adaptive change is also identified, with regions containing genes possibly associated to immunity, skin pigmentation, and reproduction (Paper IV).

This thesis demonstrates the benefit of modern theoretical and molecular tools for monitoring diversity in highly substructured population systems. These tools are relevant for advancing population genetic knowledge, as well as for sustainable management and conservation of a wide range of species.

The sympatric existence of genetically distinguishable populations of the same species remains a puzzle in ecology. Coexisting salmonid fish populations are known from over 100 freshwater lakes. Most studies of sympatric populations have used limited numbers of genetic markers making it unclear if genetic divergence involves certain parts of the genome. We returned to the first reported case of salmonid sympatry, initially detected through contrasting homozygosity at a single allozyme locus (coding for lactate dehydrogenase A) in brown trout in the small Lakes Bunnersjöarna, Sweden. First, we verified the existence of the two coexisting demes using a 96-SNP fluidigm array. We then applied whole-genome resequencing of pooled DNA to explore genome-wide diversity within and between these demes; nucleotide diversity was higher in deme I than in deme II. Strong genetic divergence is observed with genome-wide F_ST ≈ 0.2. Compared with data from populations of similar small lakes, this divergence is of similar magnitude as that between reproductively isolated populations. Individual whole-genome resequencing of two individuals per deme suggests higher inbreeding in deme II versus deme I, indicating different degree of isolation. We located two gene-copies for LDH-A and found divergence between demes in a regulatory section of one of these genes. However, we did not find a perfect fit between the sequence data and previous allozyme results, and this will require further research. Our data demonstrates genome-wide divergence governed mostly by genetic drift but also by diversifying selection in coexisting populations. This type of hidden biodiversity needs consideration in conservation management.

Developing genomic insights is challenging in nonmodel species for which resources are often scarce and prohibitively costly. Here, we explore the potential of a recently established approach using Pool-seq data to generate a de novo genome assembly for mining exons, upon which Pool-seq data are used to estimate population divergence and diversity. We do this for two pairs of sympatric populations of brown trout (Salmo trutta): one naturally sympatric set of populations and another pair of populations introduced to a common environment. We validate our approach by comparing the results to those from markers previously used to describe the populations (allozymes and individual-based single nucleotide polymorphisms [SNPs]) and from mapping the Pool-seq data to a reference genome of the closely related Atlantic salmon (Salmo salar). We find that genomic differentiation (F-ST) between the two introduced populations exceeds that of the naturally sympatric populations (F-ST = 0.13 and 0.03 between the introduced and the naturally sympatric populations, respectively), in concordance with estimates from the previously used SNPs. The same level of population divergence is found for the two genome assemblies, but estimates of average nucleotide diversity differ (pi over bar approximate to 0.002 and pi over bar approximate to 0.001 when mapping to S. trutta and S. salar, respectively), although the relationships between population values are largely consistent. This discrepancy might be attributed to biases when mapping to a haploid condensed assembly made of highly fragmented read data compared to using a high-quality reference assembly from a divergent species. We conclude that the Pool-seq-only approach can be suitable for detecting and quantifying genome-wide population differentiation, and for comparing genomic diversity in populations of nonmodel species where reference genomes are lacking.

The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar-built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re-form within a few weeks or months, thereby re-isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within-population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes Eda and Pitx1 and elemental composition (%P) varies within and among populations. Despite strong gene flow, we detected evidence for divergence in stickleback defensive traits and Eda genotypes associated with predation regime. However, this among-population variation was lower than that observed among other stickleback populations exposed to divergent predator regimes. In addition, within-population variation was very high as compared to populations from environmentally stable locations. Elemental composition was strongly associated with armor traits, Eda genotype and the presence of predators, thus suggesting that spatiotemporal variation in armor traits generates corresponding variation in elemental phenotypes. We conclude that gene flow, and especially temporal environmental variation, can maintain high levels of within-population variation while reducing, but not eliminating, among-population variation driven by spatial environmental variation.