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Ecological drivers and genetic signatures of evolutionary divergence and local adaptation in pike (Esox lucius)
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science.ORCID iD: 0000-0002-3145-1475
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The diversity among species, populations, and individuals in nature is astonishing. Genetic and phenotypic variation constitutes the raw material for evolution. It influences how populations respond to changing environments, and can impact long-term survival of species and ecosystem functioning. In this thesis I used field observations, laboratory experiments, and population genetic studies to explore how environmental conditions and eco-evolutionary processes influence genetic and phenotypic variation within and among populations of three ecotypes of pike (Esox lucius).

The results indicate that a complex interplay of geography, divergent selection, gene flow, developmental plasticity, stochastic events, and consequences of admixture has influenced patterns of diversity. Results further suggest that the importance of different processes differ for neutral and adaptive genetic variation, and within and among ecotypes. Neutral differentiation mainly varied according to gene flow and time since divergence, whilst adaptive differentiation appeared to be explained by latitude, likely in part reflecting adaptations to salinity and temperature.

The role of salinity and temperature was further evidenced by population-specific adaptations detected in the laboratory experiments, and by the identification of candidate genes previously shown to be associated with these environmental variables. The experiments also uncovered differences in within-population phenotypic responses to salinity and temperature, indicating that some populations might be predisposed to cope with environmental changes. Because of local adaptations, spawning in foreign habitats likely incur costs for individuals. This, in combination with the finding that none of the populations responded positively to admixture, might explain the persistence of the natal homing behaviour in anadromous pike.

These studies illustrate how fundamental ecological and evolutionary processes influence genetic and phenotypic diversity in pike, and exemplify how the effects can vary depending on spatiotemporal heterogeneity, level of organization (within and among ecotypes), and differ between neutral and adaptive genetic variation. Perhaps the most novel realization was that the effects of admixture for a population combination can vary depending on the origin of the male and female, respectively, which further complicates conservation measures. Overall, these findings illustrate the intricacy of the mechanisms that shape patterns of biological diversity, and highlight the importance of considering adaptive variation in management.

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2020. , p. 48
Series
Linnaeus University Dissertations ; 383/2020
Keywords [en]
adaptation, differentiation, Esox lucius, evolution, gene flow, genetic admixture, genetic structure, microsatellites, pike, RADseq, salinity tolerance, temperature tolerance
National Category
Biological Sciences
Research subject
Natural Science, Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-97310Libris ID: bn624xv7853rvrpsISBN: 978-91-89081-58-1 (print)ISBN: 978-91-89081-59-8 (electronic)OAI: oai:DiVA.org:lnu-97310DiVA, id: diva2:1455401
Public defence
2020-05-20, Fullriggaren, Hus Magna, Kalmar, 09:30 (Swedish)
Opponent
Supervisors
Available from: 2020-07-24 Created: 2020-07-24 Last updated: 2025-02-27Bibliographically approved
List of papers
1. Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for pike (Esox lucius) and a synthesis of previous studies
Open this publication in new window or tab >>Comparing the performance of microsatellites and RADseq in population genetic studies: analysis of data for pike (Esox lucius) and a synthesis of previous studies
2020 (English)In: Frontiers in Genetics, E-ISSN 1664-8021, Vol. 11, p. 1-17, article id 218Article in journal (Refereed) Published
Abstract [en]

Population genetic studies reveal biodiversity patterns and inform about drivers of evolutionary differentiation and adaptation, including gene flow, drift and selection. This can advance our understanding and aid decision making regarding management and conservation efforts. Microsatellites have long been used in population genetic studies. Thanks to the development of newer techniques, sequencing approaches such as restriction site associated DNA sequencing (RADseq) are on their way to replace microsatellites for some applications. However, the performance of these two marker types in population genetics have rarely been systematically compared. We utilized three neutrally and adaptively differentiated populations of anadromous pike (Esox lucius) to assess the relative performance of microsatellites and RADseq with respect to resolution and conclusiveness of estimates of population differentiation and genetic structure. To this end, the same set of individuals (N = 64) were genotyped with both RADseq and microsatellite markers. To assess effects of sample size, the same subset of 10 randomly chosen individuals from each population (N = 30 in total) were also genotyped with both methods. Comparisons of estimated genetic diversity and structure showed that both markers were able to uncover genetic structuring. The full RADseq dataset provided the clearest detection of the finer scaled genetic structuring, and the other three datasets (full and subset microsatellite, and subset RADseq) provided comparable results. A search for outlier loci performed on the full SNP dataset pointed to signs of selection potentially associated with salinity and temperature, exemplifying the utility of RADseq to inform about the importance of different environmental factors. To evaluate whether performance differences between the markers are general or context specific, the results of previous studies that have investigated population structure using both marker types were synthesized. The synthesis revealed that RADseq performed as well as, or better than microsatellites in detecting genetic structuring in the included studies. The differences in the ability to detect population structure, both in the present and the previous studies, are likely explained by the higher number of loci typically utilized in RADseq compared to microsatellite analysis, as increasing the number of markers will (regardless of the marker type) increase power and allow for clearer detection and higher resolution of genetic structure.

Place, publisher, year, edition, pages
Frontiers Media S.A., 2020
Keywords
adaptation, differentiation, Esox lucius, genetic structure, microsatellites, RADseq
National Category
Evolutionary Biology
Research subject
Natural Science, Ecology; Ecology, Evolutionary Biology
Identifiers
urn:nbn:se:lnu:diva-93451 (URN)10.3389/fgene.2020.00218 (DOI)000525590400001 ()32231687 (PubMedID)2-s2.0-85082700954 (Scopus ID)
Funder
Swedish Research Council Formas, 2017-00346
Available from: 2020-04-15 Created: 2020-04-15 Last updated: 2025-09-23Bibliographically approved
2. Sex-specific effects of outbreeding on offspring quality in pike (Esox lucius)
Open this publication in new window or tab >>Sex-specific effects of outbreeding on offspring quality in pike (Esox lucius)
2018 (English)In: Ecology and Evolution, E-ISSN 2045-7758, Vol. 8, no 21, p. 10448-10459Article in journal (Refereed) Published
Abstract [en]

Intraspecific genetic admixture occurs when previously separated populations withina species start interbreeding, and it can have either positive, negative, or neutral effectson reproductive performance. As there currently is no reliable predictor for theoutcome of admixture, an increased knowledge about admixture effects in differentspecies and populations is important to increase the understanding about what determinesthe response to admixture. We tested for effects of admixture on F1 offspringquality in three subpopulations of pike (Esox lucius). Gametes were collected inthe field, and eggs from each female were experimentally fertilized with milt from amale from each population (one “pure” and two “admixed” treatments). Three offspringquality measures (hatching success, fry survival, and fry length) were determinedand compared between (a) pure and admixed population combinations and (b)the sex-specifictreatments within each admixed population combination (based onthe origin of the male and female, respectively). The results suggested that althoughthere were no overall effects of admixture on offspring quality, the consequences fora given population combination could be sex-specificand thus differ depending onwhich of the parents originated from one or the other population. All offspring qualitytraits were influenced by both maternal ID and paternal ID. Sex-andindividual-specificeffects can have implications for dispersal behavior and gene flow betweennatural populations, and are important to consider in conservation efforts.

Place, publisher, year, edition, pages
Wiley-Blackwell, 2018
National Category
Evolutionary Biology Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-78895 (URN)10.1002/ece3.4510 (DOI)000450351400008 ()30464817 (PubMedID)2-s2.0-85054334923 (Scopus ID)
Funder
Swedish Research Council Formas, 2017-00346Lars Hierta Memorial Foundation, FO2017-0113Ecosystem dynamics in the Baltic Sea in a changing climate perspective - ECOCHANGE
Available from: 2018-11-20 Created: 2018-11-20 Last updated: 2025-09-23Bibliographically approved
3. Variation in salinity tolerance between and within anadromous subpopulations of pike (Esox lucius)
Open this publication in new window or tab >>Variation in salinity tolerance between and within anadromous subpopulations of pike (Esox lucius)
Show others...
2018 (English)In: Scientific Reports, E-ISSN 2045-2322, Vol. 8, article id 22Article in journal (Refereed) Published
Abstract [en]

Environmental heterogeneity is a key determinant of genetic and phenotypic diversity. Stable andhomogenous environments tends to result in evolution of specialism and local adaptations, whiletemporally unpredictable environments may maintain a diversity of specialists, promote generaliststrategies, or favour diversified bet hedging strategies. We compared salinity tolerance between twoanadromous subpopulations of pike (Esox Lucius) that utilize freshwater spawning sites with differentsalinity regimes. Eggs from each population were artificially fertilized and incubated in a salinitygradient (0, 3, 5, 7, and 9 psu) using a split-brood design. Effects on embryonic development, hatchingsuccess, survival of larvae, and fry body length were compared between populations and families.The population naturally spawning in the stable freshwater habitat showed signs of specialization forfreshwater spawning. The population exposed to fluctuating selective pressure in a spawning area withoccasional brackish water intrusions tolerated higher salinities and displayed considerable variation inreaction norms. Genetic differences and plasticity of salinity tolerance may enable populations to copewith changes in salinity regimes associated with future climate change. That geographically adjacentsubpopulations can constitute separate units with different genetic characteristics must be consideredin management and conservation efforts to avoid potentially negative effects of genetic admixture onpopulation fitness and persistence.

Place, publisher, year, edition, pages
Nature Publishing Group, 2018
National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-69620 (URN)10.1038/s41598-017-18413-8 (DOI)000419441300022 ()29311634 (PubMedID)2-s2.0-85040446275 (Scopus ID)
Note

Author Correction: https://doi.org/10.1038/s41598-018-24805-1

The original version of this Article contained an error in the title of the paper, where the word “lucius” was incorrectly given as “1ucius”. This has now been corrected in the PDF and HTML versions of the Article.

Available from: 2018-01-08 Created: 2018-01-08 Last updated: 2025-09-23Bibliographically approved
4. Adaptations of early development to local spawning temperature in anadromous populations of pike (Esox lucius)
Open this publication in new window or tab >>Adaptations of early development to local spawning temperature in anadromous populations of pike (Esox lucius)
2019 (English)In: BMC Evolutionary Biology, E-ISSN 1471-2148, Vol. 19, p. 1-13, article id 148Article in journal (Refereed) Published
Abstract [en]

Background: In the wake of climate change many environments will be exposed to increased and more variable temperatures. Knowledge about how species and populations respond to altered temperature regimes is therefore important to improve projections of how ecosystems will be affected by global warming, and to aid management. We conducted a common garden, split-brood temperature gradient (4.5 degrees C, 9.7 degrees C and 12.3 degrees C) experiment to study the effects of temperature in two populations (10 families from each population) of anadromous pike (Esox lucius) that normally experience different temperatures during spawning. Four offspring performance measures (hatching success, day degrees until hatching, fry survival, and fry body length) were compared between populations and among families. Results: Temperature affected all performance measures in a population-specific manner. Low temperature had a positive effect on the Harfjarden population and a negative effect on the Lervik population. Further, the effects of temperature differed among families within populations. Conclusions: The population-specific responses to temperature indicate genetic differentiation in developmental plasticity between populations, and may reflect an adaptation to low temperature during early fry development in Harfjarden, where the stream leading up to the wetland dries out relatively early in the spring, forcing individuals to spawn early. The family-specific responses to temperature treatment indicate presence of genetic variation for developmental plasticity (G x E) within both populations. Protecting between- and within-population genetic variation for developmental plasticity and high temperature-related adaptive potential of early life history traits will be key to long-term viability and persistence in the face of continued climate change.

Place, publisher, year, edition, pages
BioMed Central, 2019
Keywords
Adaptation, Climate change, Esox lucius, Pike, Temperature
National Category
Ecology
Research subject
Natural Science, Ecology
Identifiers
urn:nbn:se:lnu:diva-88774 (URN)10.1186/s12862-019-1475-3 (DOI)000476717300001 ()31331267 (PubMedID)2-s2.0-85069786399 (Scopus ID)
Available from: 2019-08-28 Created: 2019-08-28 Last updated: 2025-09-23Bibliographically approved

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Doctoral Dissertation (Comprehensive Summary)(5986 kB)577 downloads
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Citation style
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  • Other locale
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Output format
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