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Exploring a Pool-seq-only approach for gaining population genomic insights in nonmodel species
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0003-0296-0577
Stockholm University, Science for Life Laboratory (SciLifeLab). Stockholm University, Faculty of Science, Department of Biochemistry and Biophysics.
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Number of Authors: 102019 (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.

Place, publisher, year, edition, pages
2019. Vol. 9, p. 11448-11463
Keywords [en]
genetic diversity, genome sequencing, population genomics, Salmo trutta, salmonid, single nucleotide polymorphism
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-175045DOI: 10.1002/ece3.5646ISI: 000487783000001OAI: oai:DiVA.org:su-175045DiVA, id: diva2:1366447
Available from: 2019-10-29 Created: 2019-10-29 Last updated: 2024-01-17Bibliographically approved
In thesis
1. Genomic dynamics over contemporary time frames in wild salmonid populations
Open this publication in new window or tab >>Genomic dynamics over contemporary time frames in wild salmonid populations
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
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:nbn:se:su:diva-204219 (URN)978-91-7911-910-2 (ISBN)978-91-7911-911-9 (ISBN)
Public defence
2022-06-13, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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Available from: 2022-05-19 Created: 2022-04-28 Last updated: 2022-05-10Bibliographically approved

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Kurland, SaraWheat, Christopher W.Celorio Mancera, Maria de la PazKutschera, Verena E.Hill, JasonAndersson, AnastasiaRyman, NilsLaikre, Linda

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