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Saha, A., Kurland, S., Kutschera, V. E., Díez-del-Molino, D., Ekman, D., Ryman, N. & Laikre, L. (2024). Monitoring genome-wide diversity over contemporary time with new indicators applied to Arctic charr populations. Conservation Genetics
Open this publication in new window or tab >>Monitoring genome-wide diversity over contemporary time with new indicators applied to Arctic charr populations
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2024 (English)In: Conservation Genetics, ISSN 1566-0621, E-ISSN 1572-9737Article in journal (Refereed) Epub ahead of print
Abstract [en]

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.

Keywords
Adaptive potential, Genetic monitoring, CBD, WGS, Genetic indicators, EBVs, Salmonid
National Category
Zoology Genetics
Identifiers
urn:nbn:se:su:diva-226065 (URN)10.1007/s10592-023-01586-3 (DOI)001145706500001 ()2-s2.0-85182671789 (Scopus ID)
Available from: 2024-02-12 Created: 2024-02-12 Last updated: 2024-02-12
Hössjer, O., Laikre, L. & Ryman, N. (2023). Assessment of the Global Variance Effective Size of Subdivided Populations, and Its Relation to Other Effective Sizes. Acta Biotheoretica, 71(3), Article ID 19.
Open this publication in new window or tab >>Assessment of the Global Variance Effective Size of Subdivided Populations, and Its Relation to Other Effective Sizes
2023 (English)In: Acta Biotheoretica, ISSN 0001-5342, E-ISSN 1572-8358, Vol. 71, no 3, article id 19Article in journal (Refereed) Published
Abstract [en]

The variance effective population size (N-eV) is frequently used to quantify the expected rate at which a population's allele frequencies change over time. The purpose of this paper is to find expressions for the global N-eV of a spatially structured population that are of interest for conservation of species. Since N-eV depends on allele frequency change, we start by dividing the cause of allele frequency change into genetic drift within subpopulations (I) and a second component mainly due to migration between subpopulations (II). We investigate in detail how these two components depend on the way in which subpopulations are weighted as well as their dependence on parameters of the model such a migration rates, and local effective and census sizes. It is shown that under certain conditions the impact of II is eliminated, and N-eV of the metapopulation is maximized, when subpopulations are weighted proportionally to their long term reproductive contributions. This maximal N-eV is the sought for global effective size, since it approximates the gene diversity effective size N-eGD, a quantifier of the rate of loss of genetic diversity that is relevant for conservation of species and populations. We also propose two novel versions of N-eV, one of which (the backward version of N-eV) is most stable, exists for most populations, and is closer to N-eGD than the classical notion of N-eV. Expressions for the optimal length of the time interval for measuring genetic change are developed, that make it possible to estimate any version of N-eV with maximal accuracy.

Keywords
Genetic diversity, Length of time interval, Matrix analytic recursions, Metapopulation, Migration-drift equilibrium, Perturbation theory of matrices, Variance effective size
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:su:diva-221119 (URN)10.1007/s10441-023-09470-w (DOI)001032489500001 ()37458852 (PubMedID)2-s2.0-85158004417 (Scopus ID)
Available from: 2023-09-19 Created: 2023-09-19 Last updated: 2023-09-19Bibliographically approved
Kurland, S., Ryman, N., Hössjer, O. & Laikre, L. (2023). Effects of subpopulation extinction on effective size (Ne) of metapopulations. Conservation Genetics, 24(4), 417-433
Open this publication in new window or tab >>Effects of subpopulation extinction on effective size (Ne) of metapopulations
2023 (English)In: Conservation Genetics, ISSN 1566-0621, E-ISSN 1572-9737, Vol. 24, no 4, p. 417-433Article in journal (Refereed) Published
Abstract [en]

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 (Ne), which quantifies the rate at which genetic diversity within populations is lost. Ne 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 Ne of interconnected populations (metapopulations). Here, we apply such tools to investigate how extinction of subpopulations affects Ne of the metapopulation (NeMeta) and of separate surviving subpopulations (NeRx) 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 NeMeta 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, NeRx 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. 

Keywords
Inbreeding effective population size, Eigenvalue effective size, Realized effective size, Substructured populations, Conservation genetics
National Category
Genetics Ecology
Identifiers
urn:nbn:se:su:diva-216315 (URN)10.1007/s10592-023-01510-9 (DOI)000953077900002 ()2-s2.0-85150289396 (Scopus ID)
Available from: 2023-04-12 Created: 2023-04-12 Last updated: 2023-10-04Bibliographically approved
Kurland, S., Saha, A., P. Keehnen, N. L., Celorio-Mancera, M. d., Diez-del-Molino, D., Ryman, N. & Laikre, L. (2023). New indicators for monitoring genetic diversity applied to alpine brown trout populations using whole genome sequence data. Molecular Ecology
Open this publication in new window or tab >>New indicators for monitoring genetic diversity applied to alpine brown trout populations using whole genome sequence data
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2023 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294XArticle in journal (Refereed) Epub ahead of print
Abstract [en]

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. 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 (FROH) 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.

Keywords
biodiversity, EBVs, indicators of genetic diversity, microevolution, population genomics, temporal genetic variation
National Category
Ecology
Identifiers
urn:nbn:se:su:diva-224675 (URN)10.1111/mec.17213 (DOI)001114869500001 ()38014725 (PubMedID)2-s2.0-85178076867 (Scopus ID)
Available from: 2023-12-19 Created: 2023-12-19 Last updated: 2023-12-19
Dussex, N., Kurland, S., Olsen, R.-A., Spong, G., Ericsson, G., Ekblom, R., . . . Laikre, L. (2023). Range-wide and temporal genomic analyses reveal the consequences of near-extinction in Swedish moose. Communications Biology, 6(1), Article ID 1035.
Open this publication in new window or tab >>Range-wide and temporal genomic analyses reveal the consequences of near-extinction in Swedish moose
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2023 (English)In: Communications Biology, E-ISSN 2399-3642, Vol. 6, no 1, article id 1035Article in journal (Refereed) Published
Abstract [en]

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.

National Category
Genetics Ecology
Identifiers
urn:nbn:se:su:diva-224297 (URN)10.1038/s42003-023-05385-x (DOI)001097463800001 ()37848497 (PubMedID)2-s2.0-85174459749 (Scopus ID)
Available from: 2023-12-07 Created: 2023-12-07 Last updated: 2023-12-07Bibliographically approved
Kurland, S., Rafati, N., Ryman, N. & Laikre, L. (2022). Genomic dynamics of brown trout populations released to a novel environment. Ecology and Evolution, 12(7), Article ID e9050.
Open this publication in new window or tab >>Genomic dynamics of brown trout populations released to a novel environment
2022 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 12, no 7, article id e9050Article in journal (Refereed) Published
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 the genomic effects of population translocations. In 1979, fish from each of two genetically (FST = 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.

Keywords
conservation genetics, genetic monitoring, hybridization, population translocations, whole-genome sequencing
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-207448 (URN)10.1002/ece3.9050 (DOI)000820127600001 ()
Available from: 2022-07-26 Created: 2022-07-26 Last updated: 2024-01-17Bibliographically approved
Andersson, A., Karlsson, S., Ryman, N. & Laikre, L. (2022). Monitoring genetic diversity with new indicators applied to an alpine freshwater top predator. Molecular Ecology, 31(24), 6422-6439
Open this publication in new window or tab >>Monitoring genetic diversity with new indicators applied to an alpine freshwater top predator
2022 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 31, no 24, p. 6422-6439Article in journal (Refereed) Published
Abstract [en]

Genetic diversity is the basis for population adaptation and long-term survival, yet rarely considered in biodiversity monitoring. One key issue is the need for useful and straightforward indicators of genetic diversity. We monitored genetic diversity over 40 years (1970–2010) in metapopulations of brown trout (Salmo trutta) inhabiting 27 small mountain lakes representing 10 lake systems in central Sweden using >1200 fish per time point. We tested six newly proposed indicators; three were designed for broad, international use in the UN Convention on Biological Diversity (CBD) and are currently applied in several countries. The other three were recently elaborated for national use by a Swedish science-management effort and applied for the first time here. The Swedish indicators use molecular genetic data to monitor genetic diversity within and between populations (indicators ΔH and ΔFST, respectively) and assess the effective population size (Ne-indicator). We identified 29 genetically distinct populations, all retained over time. Twelve of the 27 lakes harboured more than one population indicating that brown trout biodiversity hidden as cryptic, sympatric populations are more common than recognized. The Ne indicator showed values below the threshold (Ne ≤ 500) in 20 populations with five showing Ne < 100. Statistically significant genetic diversity reductions occurred in several populations. Metapopulation structure appears to buffer against diversity loss; applying the indicators to metapopulations suggest mostly acceptable rates of change in all but one system. The CBD indicators agreed with the Swedish ones but provided less detail. All these indicators are appropriate for managers to initiate monitoring of genetic biodiversity. 

Keywords
cryptic sympatry, hidden biodiversity, intraspecific biodiversity, protected area, sympatric populations
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-212623 (URN)10.1111/mec.16710 (DOI)000867482800001 ()2-s2.0-85139767518 (Scopus ID)
Available from: 2022-12-09 Created: 2022-12-09 Last updated: 2022-12-09Bibliographically approved
Laikre, L., Allendorf, F. W., Aspi, J., Carroll, C., Dalén, L., Fredrickson, R., . . . Vucetich, J. A. (2022). Planned cull endangers Swedish wolf population. Science, 377(6602)
Open this publication in new window or tab >>Planned cull endangers Swedish wolf population
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2022 (English)In: Science, ISSN 0036-8075, E-ISSN 1095-9203, Vol. 377, no 6602Article in journal (Refereed) Published
Abstract [en]

In May, the Swedish Parliament announced a goal to reduce the Swedish wolf population from about 400 to about 200 individuals (1). This action further threatens this highly endangered population, which is genetically isolated and inbred. Scientific advice for improvements has not been implemented (2, 3).

The Swedish Parliament proposed this drastic cull at a time when biodiversity is a global focus. The 50-year anniversary of the first UN conference on the environment was celebrated in June, and the UN Convention on Biological Diversity (CBD) will soon finalize its global biodiversity framework for 2020 to 2050. Sweden’s actions are inconsistent with the country’s obligations under the CBD and European Union law.

Few wild populations are as well studied as the Scandinavian wolf. Genetic monitoring has provided a full pedigree since the population was reestablished in the 1980s after extinction, and the data confirm persisting genetic isolation (4–6). Hunting, conducted both legally and illegally, has prevented population expansion and the influx of genetic variation.

Three founders comprised the population’s genetic origin until 2007, and only three more wolves have subsequently contributed genetically to the present population (6). The genetic base is thus extremely narrow, and genomic erosion has been confirmed (7, 8). The average level of inbreeding is similar to the level found in the offspring of two full siblings (6). Inbreeding in this population has been shown to reduce litter size (4). Also, high frequencies of anatomical defects (9) and male reproductive disorders (10) have been observed.

To make this population viable, population size and immigration must increase. So far, the population has been too small, and limited immigration followed by inbreeding could lead to extinction, similar to the Isle Royale wolf population (11). The goal should be to recreate a well-connected metapopulation spanning Scandinavia and Finland with a genetically effective population size of over 500, in line with the proposed CBD indicator (12). Considerably more genetic exchange than the current one-migrant-per-generation aim is needed (3).

Keywords
animal culling, animal hunting, biodiversity, endangered species, gene isolation, inbreeding, Letter, litter size, nonhuman, pedigree, population dynamics, species extinction, Sweden, wolf, animal, Animals, Wolves
National Category
Zoology
Identifiers
urn:nbn:se:su:diva-212109 (URN)10.1126/science.add5299 (DOI)000822228900027 ()35857558 (PubMedID)2-s2.0-85133948503 (Scopus ID)
Available from: 2022-12-01 Created: 2022-12-01 Last updated: 2022-12-01Bibliographically approved
Saha, A., Andersson, A., Kurland, S., Pruisscher Keehnen, N. L., Kutschera, V. E., Hössjer, O., . . . Laikre, L. (2022). Whole-genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes. Molecular Ecology, 31(2), 498-511
Open this publication in new window or tab >>Whole-genome resequencing confirms reproductive isolation between sympatric demes of brown trout (Salmo trutta) detected with allozymes
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2022 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 31, no 2, p. 498-511Article in journal (Refereed) Published
Abstract [en]

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 FST ≈ 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.

Keywords
coexisting populations, conservation genetics, conservation genomics, hidden biodiversity, population genetic structure, salmonid
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-200014 (URN)10.1111/mec.16252 (DOI)000718735900001 ()34699656 (PubMedID)
Available from: 2021-12-22 Created: 2021-12-22 Last updated: 2022-01-25Bibliographically approved
Dussex, N., Alberti, F., Heino, M. T., Olsen, R.-A., van der Valk, T., Ryman, N., . . . Díez-del-Molino, D. (2020). Moose genomes reveal past glacial demography and the origin of modern lineages. BMC Genomics, 21(1), Article ID 854.
Open this publication in new window or tab >>Moose genomes reveal past glacial demography and the origin of modern lineages
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2020 (English)In: BMC Genomics, E-ISSN 1471-2164, Vol. 21, no 1, article id 854Article in journal (Refereed) Published
Abstract [en]

Background: Numerous megafauna species from northern latitudes went extinct during the Pleistocene/Holocene transition as a result of climate-induced habitat changes. However, several ungulate species managed to successfully track their habitats during this period to eventually flourish and recolonise the holarctic regions. So far, the genomic impacts of these climate fluctuations on ungulates from high latitudes have been little explored. Here, we assemble a de-novo genome for the European moose (Alces alces) and analyse it together with re-sequenced nuclear genomes and ancient and modern mitogenomes from across the moose range in Eurasia and North America.

Results: We found that moose demographic history was greatly influenced by glacial cycles, with demographic responses to the Pleistocene/Holocene transition similar to other temperate ungulates. Our results further support that modern moose lineages trace their origin back to populations that inhabited distinct glacial refugia during the Last Glacial Maximum (LGM). Finally, we found that present day moose in Europe and North America show low to moderate inbreeding levels resulting from post-glacial bottlenecks and founder effects, but no evidence for recent inbreeding resulting from human-induced population declines.

Conclusions: Taken together, our results highlight the dynamic recent evolutionary history of the moose and provide an important resource for further genomic studies.

Keywords
Genomics, Moose, Ancient DNA, Phylogeny, Demography
National Category
Environmental Biotechnology Biological Sciences
Identifiers
urn:nbn:se:su:diva-189179 (URN)10.1186/s12864-020-07208-3 (DOI)000597320300001 ()33267779 (PubMedID)
Available from: 2021-01-21 Created: 2021-01-21 Last updated: 2024-01-17Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0003-3342-8479

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