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Small-scale population divergence is driven by local larval environment in a temperate amphibian
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0001-6737-1488
Department of Ecology and Evolution, Le Biophore, Université de Lausanne,.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Department of Ecology, Box 7044, Swedish University of Agricultural Sciences.ORCID iD: 0000-0003-0954-7312
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2021 (English)In: Human Heredity, ISSN 0001-5652, E-ISSN 1423-0062, Vol. 126, no 2, p. 279-292Article in journal (Refereed) Published
Abstract [en]

Genomic variation within and among populations is shaped by the interplay between natural selection and the effects of genetic drift and gene flow. Adaptive divergence can be found in small-scale natural systems even when population sizes are small, and the potential for gene flow is high, suggesting that local environments exert selection pressures strong enough to counteract the opposing effects of drift and gene flow. Here, we investigated genomic differentiation in nine moor frog (Rana arvalis) populations in a small-scale network of local wetlands using 16,707 ddRAD-seq SNPs, relating levels of differentiation with local environments, as well as with properties of the surrounding landscape. We characterized population structure and differentiation, and partitioned the effects of geographic distance, local larval environment, and landscape features on total genomic variation. We also conducted gene-environment association studies using univariate and multivariate approaches. We found small-scale population structure corresponding to 6-8 clusters. Local larval environment was the most influential component explaining 2.3% of the total genetic variation followed by landscape features (1.8%) and geographic distance (0.8%), indicative of isolation-by-environment, -by-landscape, and -by-distance, respectively. We identified 1000 potential candidate SNPs putatively under divergent selection mediated by the local larval environment. The candidate SNPs were involved in, among other biological functions, immune system function and development. Our results suggest that small-scale environmental differences can exert selection pressures strong enough to counteract homogenizing effects of gene flow and drift in this small-scale system, leading to observable population differentiation.

Place, publisher, year, edition, pages
2021. Vol. 126, no 2, p. 279-292
Keywords [en]
Adaptive divergence, gene flow, amphibians
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-390998DOI: 10.1038/s41437-020-00371-zISI: 000571688700001PubMedID: 32958927OAI: oai:DiVA.org:uu-390998DiVA, id: diva2:1343474
Funder
Swedish Research Council, 621-2013-4503Available from: 2019-08-16 Created: 2019-08-16 Last updated: 2021-04-19Bibliographically approved
In thesis
1. Population divergence at different spatial scales in a wide-spread amphibian
Open this publication in new window or tab >>Population divergence at different spatial scales in a wide-spread amphibian
2019 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

To study the distribution of genetic and phenotypic variation in different environments and at different spatial scales is important in order to understand the process of local adaptation and how populations will respond to future climate change. In my thesis I study populations of moor frogs (Rana arvalis) at different spatial scales, first along a 1700 km latitudinal gradient (Paper I, II, IV) and, second, in a system of inter-connected wetlands (III, IV). In Paper I, I present evidence for a major latitudinal break-point in larval life-history traits which is linked to a post glacial contact zone between two lineages that colonized Scandinavia after the last ice age. Using QST-FST comparisons I found divergent selection acting on life-history traits, where a major source of differentiation comes from the two colonization routes. In Paper II I focus on genomic variation, demographic history and selection along the gradient. Using demographic modeling I confirm the proposed demographic history and show historical signatures of gene flow between regions and over the contact zone. In terms of genetic variation showing extreme differentiation as well as associations with growing season length I identify numerous variants under putative divergent selection, some of which have functions relating to immunity and development. I further show that differentiation outlier variation is higher in the north, as compared to neutral variation and variation associated with growing season length, which both decrease with latitude. These patterns are shaped by gene flow over the contact zone and the increased strength of drift at higher latitudes. I reduce the spatial scale in Paper III and characterize larval environments, landscape and geographical distance, to partition their influence on genetic variation. I show that environment explained more of the genetic variation than landscape and geographic distance, indicating that adaptive divergence can persist under high gene flow. Using the environmental variables, I identify genetic variants under putative divergent selection with functions associated with development and immunity. Using data from both scales, QST-FST comparisons and gene-phenotype associations I show in Paper IV that selection on both larval traits aligns across scales, whereas selection on plasticity only aligns in size at metamorphosis. This further connects to the influence of temperature and seasonal time constraints in colder environments. Finally, I find several genetic variants associated with the traits and plasticity at both spatial scales with functions relating to immunity and metamorphosis.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2019. p. 53
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1841
Keywords
Adaptive divergence, environmental gradients, genomics, life-history, amphibians
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-391039 (URN)978-91-513-0723-7 (ISBN)
Public defence
2019-09-20, Zootissalen, EBC, Villavägen 9, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2019-08-29 Created: 2019-08-16 Last updated: 2019-09-17Bibliographically approved

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