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Genomic dynamics over contemporary time frames in wild salmonid populations
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-5370-1236
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

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 (Ne) 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.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2022. , p. 52
Keywords [en]
Conservation genomics, genetic monitoring, whole-genome sequencing, metapopulation, salmonid, brown trout, effective population size, Pool-seq, genetic connectivity, intraspecific diversity, sympatric populations
National Category
Zoology
Research subject
Population Genetics
Identifiers
URN: urn:nbn:se:su:diva-204219ISBN: 978-91-7911-910-2 (print)ISBN: 978-91-7911-911-9 (electronic)OAI: oai:DiVA.org:su-204219DiVA, id: diva2:1654755
Public defence
2022-06-13, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
Opponent
Supervisors
Available from: 2022-05-19 Created: 2022-04-28 Last updated: 2022-05-10Bibliographically approved
List of papers
1. Effects of subpopulation extinction on effective size (Ne) of metapopulations
Open this publication in new window or tab >>Effects of subpopulation extinction on effective size (Ne) of metapopulations
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-204218 (URN)
Available from: 2022-04-27 Created: 2022-04-27 Last updated: 2022-04-28
2. Exploring a Pool-seq-only approach for gaining population genomic insights in nonmodel species
Open this publication in new window or tab >>Exploring a Pool-seq-only approach for gaining population genomic insights in nonmodel species
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2019 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 9, p. 11448-11463Article in journal (Refereed) Published
Abstract [en]

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.

Keywords
genetic diversity, genome sequencing, population genomics, Salmo trutta, salmonid, single nucleotide polymorphism
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-175045 (URN)10.1002/ece3.5646 (DOI)000487783000001 ()
Available from: 2019-10-29 Created: 2019-10-29 Last updated: 2024-01-17Bibliographically approved
3. Genomic dynamics of brown trout (Salmo trutta) populations released to a novel environment
Open this publication in new window or tab >>Genomic dynamics of brown trout (Salmo trutta) populations released to a novel environment
(English)Manuscript (preprint) (Other academic)
Abstract [en]

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 genomic effects of population translocations. In 1979, fish from each of two genetically and ecologically separate populations were released at one point in time to the same lake system. Whole-genome sequencing data is used to characterize diversity within and divergence between introduced fish from different source populations and fish inhabiting two lakes down-stream of the release sites, sampled 30 years later (c. 5 generations). Diversity and divergence among introduced populations and fish sampled in the wild c. 5 generations later suggest extensive hybridization. Introduced fish are unequally represented in the lakes down-stream of the release sites, with fish from one population mainly contributing to the lake closest to the release site, and the fish from the other dominating the lake further downstream. We also identify genomic regions putatively under directional selection in the new lake system, where genes from one of the introduced populations, regulating metabolism, appear advantageous. Our results demonstrate that genetic effects of population translocations e.g., establishment, hybridization, and adaptation can be rapid after release into novel environments – even for a species with relatively small local effective population sizes and a large, complex genome. This is an important contribution to understanding the microevolutionary effects population translocations have on intraspecific diversity.  

Keywords
Population translocations, WGS, genetic monitoring, conservation genetics, hybridization
National Category
Natural Sciences
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-204216 (URN)DOI: 10.22541/au.164863303.36499406/v1 (DOI)
Available from: 2022-04-27 Created: 2022-04-27 Last updated: 2022-04-28
4. Conservation genetic monitoring of natural brown trout (Salmo trutta) populations using whole genome resequencing data
Open this publication in new window or tab >>Conservation genetic monitoring of natural brown trout (Salmo trutta) populations using whole genome resequencing data
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Research subject
Population Genetics
Identifiers
urn:nbn:se:su:diva-204217 (URN)
Available from: 2022-04-27 Created: 2022-04-27 Last updated: 2022-04-28

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