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Population divergence at different spatial scales in a wide-spread amphibian
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
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 [en]
Adaptive divergence, environmental gradients, genomics, life-history, amphibians
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-391039ISBN: 978-91-513-0723-7 (print)OAI: oai:DiVA.org:uu-391039DiVA, id: diva2:1343533
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
List of papers
1. Post-glacial colonization routes coincide with a life-history breakpoint along a latitudinal gradient
Open this publication in new window or tab >>Post-glacial colonization routes coincide with a life-history breakpoint along a latitudinal gradient
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2019 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 32, no 4, p. 356-368Article in journal (Refereed) Published
Abstract [en]

Although adaptive divergence along environmental gradients has repeatedly been demonstrated, the role of post‐glacial colonization routes in determining phenotypic variation along gradients has received little attention. Here, we used a hierarchical QSTFST approach to separate the roles of adaptive and neutral processes in shaping phenotypic variation in moor frog (Rana arvalis) larval life histories along a 1,700 km latitudinal gradient across northern Europe. This species has colonized Scandinavia via two routes with a contact zone in northern Sweden. By using neutral SNP and common garden phenotypic data from 13 populations at two temperatures, we showed that most of the variation along the gradient occurred between the two colonizing lineages. We found little phenotypic divergence within the lineages; however, all phenotypic traits were strongly diverged between the southern and northern colonization routes, with higher growth and development rates and larger body size in the north. The QST estimates between the colonization routes were four times higher than FST, indicating a prominent role for natural selection. QST within the colonization routes did not generally differ from FST, but we found temperature‐dependent adaptive divergence close to the contact zone. These results indicate that lineage‐specific variation can account for much of the adaptive divergence along a latitudinal gradient.

Keywords
cogradient variation, colonization, countergradient variation, latitudinal gradient, life-history traits, local adaptation, Q(ST)-F-ST comparison
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-382989 (URN)10.1111/jeb.13419 (DOI)000464516900006 ()30703260 (PubMedID)
Funder
Swedish Research Council, 621-2013-4503Knut and Alice Wallenberg FoundationCarl Tryggers foundation
Available from: 2019-05-13 Created: 2019-05-13 Last updated: 2019-08-16Bibliographically approved
2. Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation
Open this publication in new window or tab >>Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 12, p. 2996-3011Article in journal (Refereed) Published
Abstract [en]

Stochastic effects from demographic processes and selection are expected to shape the distribution of genetic variation in spatially heterogeneous environments. As the amount of genetic variation is central for long‐term persistence of populations, understanding how these processes affect variation over large‐scale geographical gradients is pivotal. We investigated the distribution of neutral and putatively adaptive genetic variation, and reconstructed demographic history in the moor frog (Rana arvalis) using 136 individuals from 15 populations along a 1,700‐km latitudinal gradient from northern Germany to northern Sweden. Using double digest restriction‐site associated DNA sequencing we obtained 27,590 single nucleotide polymorphisms (SNPs), and identified differentiation outliers and SNPs associated with growing season length. The populations grouped into a southern and a northern cluster, representing two phylogeographical lineages from different post‐glacial colonization routes. Hybrid index estimation and demographic model selection showed strong support for a southern and northern lineage and evidence of gene flow between regions located on each side of a contact zone. However, patterns of past gene flow over the contact zone differed between neutral and putatively adaptive SNPs. While neutral nucleotide diversity was higher along the southern than the northern part of the gradient, nucleotide diversity in differentiation outliers showed the opposite pattern, suggesting differences in the relative strength of selection and drift along the gradient. Variation associated with growing season length decreased with latitude along the southern part of the gradient, but not along the northern part where variation was lower, suggesting stronger climate‐mediated selection in the north. Outlier SNPs included loci involved in immunity and developmental processes.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
Keywords
adaptive divergence, amphibians, divergent selection, genetic drift, range expansion, small populations
National Category
Evolutionary Biology Ecology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-390931 (URN)10.1111/mec.15132 (DOI)000475983100005 ()
Available from: 2019-08-15 Created: 2019-08-15 Last updated: 2019-09-09Bibliographically approved
3. Small-scale population divergence is driven by local larval environment in a temperate amphibian
Open this publication in new window or tab >>Small-scale population divergence is driven by local larval environment in a temperate amphibian
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Small-scale genomic variation within and among populations is shaped by the interplay between divergent selection and the opposing effects of genetic drift and gene flow. Adaptive divergence has been found in natural systems even when population sizes are small and the potential for gene flow is high, suggesting that local environments exert strong enough selection pressure to counteract the opposing effects of drift and gene flow. However, the environmental factors causing the divergence have rarely been partitioned. Here, we investigated the genetic and environmental basis of adaptive divergence in nine populations of moor frog (Rana arvalis) distributed in a small-scale network of wetlands. We measured environmental and landscape variables within and surrounding the focal ponds. Using 16707 ddRAD-seq SNPs, we characterized population structure and differentiation, partitioned the effects of geographical distance, local larval environment and the landscape on total genomic variation. We also conducted gene-environment association studies using univariate and multivariate approaches. We found small-scale population structure corresponding to between six and eight clusters. Local larval environment explained most of the total genetic variation followed by landscape features and geographic distance indicative of isolation-by-environment -by-landscape and -by-distance. We identified a fairly large number of candidate SNPs putatively under divergent selection mediated by the larval environment. The candidate SNPs are involved in immune system function and development, among other biological functions. Our results show that small scale environmental differences can in fact exert selection pressures strong enough to counteract ameliorating effects of potential gene flow and drift in this system.

Keywords
Adaptive divergence, gene flow, amphibians
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-390998 (URN)
Funder
Swedish Research Council
Available from: 2019-08-16 Created: 2019-08-16 Last updated: 2019-08-16
4. Divergence and plasticity of larval life-history align at different spatial scales in a high-latitude amphibian
Open this publication in new window or tab >>Divergence and plasticity of larval life-history align at different spatial scales in a high-latitude amphibian
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Understanding divergence and plasticity of fitness associated traits along climatic gradients is important in order to understand how populations will respond to environmental change. Here we investigated larval life history evolution of the moor frog (Rana arvalis) along two climatic gradients of contrasting spatial scale: along a 1700km latitudinal gradient and in a small-scale wetland network with contrasting environments. In both systems, we conducted a common garden experiment where we raised tadpoles in two temperature treatments and measured two larval life-history traits (larval period and mass at metamorphosis) and their plasticity. We also utilized ddRAD-seq to conduct QST-FST comparisons and genotype-phenotype association studies in both systems. In the wetland network, we found low levels of genetic differentiation, but evidence of adaptive divergence in larval period and in plasticity of mass at metamorphosis. Along the latitudinal gradient, we found strong neutral genetic differentiation and evidence of selection on trait means and their plasticity for both larval period and mass at metamorphosis. These results suggest that patterns of climatic selection on traits means and plasticity largely align across different spatial scales. Finally, we identified a number of SNPs associated with the two larval-life history traits and plasticity. Several rad-tags matched genes and proteins involved in immunity and developmental processes, pointing to the potential importance of development rate-immunity trade-offs shaping life-history evolution in temperate amphibians along climatic gradients.

Keywords
Selection, environmental gradients, time constraints, plasticity, life-history, GWAS, amphibians
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology; Biology with specialization in Animal Ecology; Biology with specialization in Animal Ecology; Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-390999 (URN)
Available from: 2019-08-16 Created: 2019-08-16 Last updated: 2019-08-16

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