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Klinga, P., Mikoláš, M., Smolko, P., Tejkal, M., Höglund, J. & Paule, L. (2019). Considering landscape connectivity and gene flow in the Anthropocene using complementary landscape genetics and habitat modelling approaches. Landscape Ecology, 34(3), 521-536
Open this publication in new window or tab >>Considering landscape connectivity and gene flow in the Anthropocene using complementary landscape genetics and habitat modelling approaches
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2019 (English)In: Landscape Ecology, ISSN 0921-2973, E-ISSN 1572-9761, Vol. 34, no 3, p. 521-536Article in journal (Refereed) Published
Abstract [en]

Context: A comprehensive understanding of how rapidly changing environments affect species gene flow is critical for mitigating future biodiversity losses. While recent methodological developments in landscape ecology and genetics have greatly advanced our understanding of biodiversity conservation, they are rarely combined and applied in studies.

Objectives: We merged multifaceted landscape habitat modelling with genetics to detect and design biological corridors, and we evaluated the importance of habitat patches to test corridor efficacy for gene flow in a fragmented landscape. We examined an isolated population of an endangered umbrella species, the capercaillie (Tetrao urogallus), in the Western Carpathians; they have experienced habitat deterioration and accompanying population declines in recent decades.

Methods: To detect spatial patterns of genetic distances, we combined and optimized resistance surfaces using species distribution modelling, structural and functional connectivity analyses, multivariate regression approaches, and Moran’s eigenvector maps at hierarchical scales.

Results: Larger habitat patches had better gene flow among them, and we confirmed a broken metapopulation network characterised by a pattern of isolation by the environment. Distance to human settlements explained landscape genetic patterns better than other environmental and landscape features, MaxEnt resistance, Conefor resistance surfaces, and the pairwise Euclidean distances among individuals. The closer individuals were to settlements, the more pronounced were the effects of logging and other negative factors on their connectivity.

Conclusions: Merging multifaceted landscape habitat modelling with genetics can effectively test corridor efficacy for gene flow, and it represents a powerful tool for conservation of endangered species.

Keywords
Landscape genetics, Fragmentation, Isolation by environment, Conservation, Tetrao urogallus
National Category
Landscape Architecture
Identifiers
urn:nbn:se:uu:diva-382667 (URN)10.1007/s10980-019-00789-9 (DOI)000463741600005 ()
Available from: 2019-05-07 Created: 2019-05-07 Last updated: 2019-05-07Bibliographically approved
Lindsay, W. R., Andersson, S., Bererhi, B., Höglund, J., Johnsen, A., Kvarnemo, C., . . . Edwards, S. V. (2019). Endless forms of sexual selection. PeerJ, 7, Article ID e7988.
Open this publication in new window or tab >>Endless forms of sexual selection
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2019 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 7, article id e7988Article in journal (Refereed) Published
Abstract [en]

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a "stock-taking'' workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the 'aesthetic sense' proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate 'null model' of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress.

Keywords
Sexual selection, Sexual conflict, Mate choice, Polyandry, Speciation, Sensory bias, Signal honesty, Sperm competition, Cryptic female choice, Epigenetics
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-397639 (URN)10.7717/peerj.7988 (DOI)000494231300007 ()31720113 (PubMedID)
Funder
Swedish Research Council
Available from: 2019-11-22 Created: 2019-11-22 Last updated: 2019-11-22Bibliographically approved
Meyer-Lucht, Y., Luquet, E., Johannesdottir, F., Mörch, P. R., Quintela, M., Richter Boix, A., . . . Laurila, A. (2019). Genetic basis of amphibian larval development along a latitudinal gradient: Gene diversity, selection and links with phenotypic variation in transcription factor C/EBP-1. Molecular Ecology, 28(11), 2786-2801
Open this publication in new window or tab >>Genetic basis of amphibian larval development along a latitudinal gradient: Gene diversity, selection and links with phenotypic variation in transcription factor C/EBP-1
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 11, p. 2786-2801Article in journal (Refereed) Published
Abstract [en]

Ectotherm development rates often show adaptive divergence along climatic gradients, but the genetic basis for this variation is rarely studied. Here, we investigated the genetic basis for phenotypic variation in larval development in the moor frog Rana arvalis from five regions along a latitudinal gradient from Germany to northern Sweden. We focused on the C/EBP-1 gene, a transcription factor associated with larval development time. Allele frequencies at C/EBP-1 varied strongly among geographical regions. Overall, the distribution of alleles along the gradient was in concordance with the dual post-glacial colonization routes into Scandinavia, with a large number of alleles exclusively present along the southern colonization route. Only three of 38 alleles were shared between the routes. Analysis of contemporary selection on C/EBP-1 showed divergent selection among the regions, probably reflecting adaptation to the local environmental conditions, although this was especially strong between southern and northern regions coinciding also with lineages from different colonization routes. Overall, the C/EBP-1 gene has historically been under purifying selection, but two specific amino acid positions showed significant signals of positive selection. These positions showed divergence between southern and northern regions, and we suggest that they are functionally involved in the climatic adaptation of larval development. Using phenotypic data from a common garden experiment, we found evidence for specific C/EBP-1 alleles being correlated with larval development time, suggesting a functional role in adaptation of larval development to large-scale climatic variation.

Place, publisher, year, edition, pages
WILEY, 2019
Keywords
adaptation, amphibians, climate change, ecological genetics, life history evolution
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-390651 (URN)10.1111/mec.15123 (DOI)000473204200007 ()31067349 (PubMedID)
Funder
Swedish Research Council, 621-2013-4503
Available from: 2019-08-13 Created: 2019-08-13 Last updated: 2019-08-13Bibliographically approved
Kozma, R., Mörch, P. R. & Höglund, J. (2019). Genomic regions of speciation and adaptation among three species of grouse. Scientific Reports, 9, Article ID 812.
Open this publication in new window or tab >>Genomic regions of speciation and adaptation among three species of grouse
2019 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 9, article id 812Article in journal (Refereed) Published
Abstract [en]

Understanding the molecular basis of adaption is one of the central goals in evolutionary biology and when investigated across sister species it can provide detailed insight into the mechanisms of speciation. Here, we sequence the genomes of 34 individuals from three closely related grouse species in order to uncover the genomic architecture of speciation and the genes involved in adaptation. We identify 6 regions, containing 7 genes that show lineage specific signs of differential selection across the species. These genes are involved in a variety of cell processes ranging from stress response to neural, gut, olfactory and limb development. Genome wide neutrality test statistics reveal a strong signal of population expansion acting across the genomes. Additionally, we uncover a 3.5 Mb region on chromosome 20 that shows considerably lower levels of differentiation across the three grouse lineages, indicating possible action of uniform selection in this region.

National Category
Genetics Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-377350 (URN)10.1038/s41598-018-36880-5 (DOI)000456826200041 ()30692562 (PubMedID)
Funder
Swedish Research Council
Available from: 2019-02-22 Created: 2019-02-22 Last updated: 2019-02-22Bibliographically approved
Mörch, P. R., Luquet, E., Meyer-Lucht, Y., Richter Boix, A., Höglund, J. & Laurila, A. (2019). Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation. Molecular Ecology, 28(12), 2996-3011
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
Luquet, E., Mörch, P. R., Cortazar-Chinarro, M., Meyer-Lucht, Y., Höglund, J. & Laurila, A. (2019). Post-glacial colonization routes coincide with a life-history breakpoint along a latitudinal gradient. Journal of Evolutionary Biology, 32(4), 356-368
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
Kärvemo, S., Laurila, A. & Höglund, J. (2019). Urban environment and reservoir host species are associated with Batrachochytrium dendrobatidis infection prevalence in the common toad. Diseases of Aquatic Organisms, 134(1), 33-42
Open this publication in new window or tab >>Urban environment and reservoir host species are associated with Batrachochytrium dendrobatidis infection prevalence in the common toad
2019 (English)In: Diseases of Aquatic Organisms, ISSN 0177-5103, E-ISSN 1616-1580, Vol. 134, no 1, p. 33-42Article in journal (Refereed) Published
Abstract [en]

Human-induced changes of the environment, including landscape alteration and habitat loss, may affect wildlife disease dynamics and have important ramifications for wildlife conservation. Amphibians are among the vertebrate taxa most threatened by anthropogenic habitat change. The emerging fungal pathogen Batrachochytrium dendrobatidis (Bd) has caused extinctions and population declines in hundreds of anuran species globally. We studied how the urban landscape is associated with the prevalence of Bd infections by sampling 655 anurans of 3 species (mainly the common toad Bufo bufo) in 42 ponds surrounded by different amounts of urban habitat (defined as towns, cities or villages). We also examined the association between Bd infections and a potential reservoir host species (the moor frog Rana arvalis). We found that 38% of the sites were positive for Bd with an infection prevalence of 4.4%. The extent of urban landscape was negatively correlated with Bd infection prevalence. However, the positive association of Bd with the presence of the possible reservoir species was substantially stronger than the urban effects. The body condition index of B. bufo was negatively associated with Bd infection. This Bd effect was stronger than the negative effect of urban landscape on body condition. Our results suggest that urban environments in Sweden have a negative impact on Bd infections, while the presence of the reservoir species has a positive impact on Bd prevalence. Our study also highlights the potential importance of Bd infection on host fitness, especially in rural landscapes.

Place, publisher, year, edition, pages
INTER-RESEARCH, 2019
Keywords
Amphibians, Chytrid, Disease transmission, Body condition, Scandinavia
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-394177 (URN)10.3354/dao03359 (DOI)000484001500004 ()
Funder
Swedish Research Council Formas, 215-2014-594
Available from: 2019-10-04 Created: 2019-10-04 Last updated: 2019-10-04Bibliographically approved
Fisher, M. C., Ghosh, P., Shelton, J. M. G., Bates, K., Brookes, L., Wierzbicki, C., . . . Garner, T. W. J. (2018). Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi. Scientific Reports, 8, Article ID 7772.
Open this publication in new window or tab >>Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi
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2018 (English)In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 8, article id 7772Article in journal (Refereed) Published
Abstract [en]

Parasitic chytrid fungi have emerged as a significant threat to amphibian species worldwide, necessitating the development of techniques to isolate these pathogens into culture for research purposes. However, early methods of isolating chytrids from their hosts relied on killing amphibians. We modified a pre-existing protocol for isolating chytrids from infected animals to use toe clips and biopsies from toe webbing rather than euthanizing hosts, and distributed the protocol to researchers as part of the BiodivERsA project RACE; here called the RML protocol. In tandem, we developed a lethal procedure for isolating chytrids from tadpole mouthparts. Reviewing a database of use a decade after their inception, we find that these methods have been applied across 5 continents, 23 countries and in 62 amphibian species. Isolation of chytrids by the non-lethal RML protocol occured in 18% of attempts with 207 fungal isolates and three species of chytrid being recovered. Isolation of chytrids from tadpoles occured in 43% of attempts with 334 fungal isolates of one species (Batrachochytrium dendrobatidis) being recovered. Together, these methods have resulted in a significant reduction and refinement of our use of threatened amphibian species and have improved our ability to work with this group of emerging pathogens.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2018
National Category
Microbiology
Identifiers
urn:nbn:se:uu:diva-356449 (URN)10.1038/s41598-018-24472-2 (DOI)000432340300001 ()29773857 (PubMedID)
Available from: 2018-08-01 Created: 2018-08-01 Last updated: 2018-08-01Bibliographically approved
Kärvemo, S., Meurling, S., Berger, D., Höglund, J. & Laurila, A. (2018). Effects of host species and environmental factors on the prevalence of Batrachochytrium dendrobatidis in northern Europe. PLoS ONE, 13(10), Article ID e0199852.
Open this publication in new window or tab >>Effects of host species and environmental factors on the prevalence of Batrachochytrium dendrobatidis in northern Europe
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2018 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 10, article id e0199852Article in journal (Refereed) Published
Abstract [en]

The fungal pathogen Batrachochytrium dendrobatidis (Bd) poses a major threat to amphibian populations. To assist efforts to address such threats, we examined differences in Bd host infection prevalence among amphibian species and its relations to both local environmental factors in breeding habitats and landscape variables measured at three scales (500, 2000 and 5000 m radii) around breeding sites in southernmost Sweden. We sampled 947 anurans of six species in 31 ponds and assessed their infection status. We then examined correlations of infection prevalence with canopy cover, pond perimeter and pH (treated as local-scale pond characteristics), and the number of ponds, area of arable land, area of mature forest, number of resident people and presence of sea within the three radii (treated as landscape variables). The Bd infection prevalence was very low, 0.5-1.0%, in two of the six anuran species (Bufo bufo and Rana temporaria), and substantially higher (13-64%) in the other four (Bombina bombina, Bufotes variabilis, Epidalea calamita, Rana arvalis). In the latter four species Bd infection prevalence was positively associated with ponds' pH (site range: 5.3-8.1), and negatively associated with areas of mature forest and/or wetlands in the surroundings. Our results show that the infection dynamics of Bd are complex and associated with host species, local pond characteristics and several landscape variables at larger spatial scales. Knowledge of environmental factors associated with Bd infections and differences in species' susceptibility may help to counter further spread of the disease and guide conservation action plans, especially for the most threatened species.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2018
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-369896 (URN)10.1371/journal.pone.0199852 (DOI)000448438400003 ()30359384 (PubMedID)
Funder
Swedish Research Council Formas, 215-2014-594Carl Tryggers foundation , 15:220, KF17:14
Available from: 2018-12-19 Created: 2018-12-19 Last updated: 2019-11-12Bibliographically approved
Kozma, R., Lillie, M., Benito, B. M., Svenning, J.-C. & Höglund, J. (2018). Past and potential future population dynamics of three grouse species using ecological and whole genome coalescent modeling. Ecology and Evolution, 8(13), 6671-6681
Open this publication in new window or tab >>Past and potential future population dynamics of three grouse species using ecological and whole genome coalescent modeling
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2018 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, no 13, p. 6671-6681Article in journal (Other academic) Published
Abstract [en]

Studying demographic history of species provides insight into how the past has shaped the current levels of overall biodiversity and genetic composition of species, but also how these species may react to future perturbations. Here we investigated the demographic history of the willow grouse (Lagopus lagopus), rock ptarmigan (Lagopus muta), and black grouse (Tetrao tetrix) through the Late Pleistocene using two complementary methods and whole genome data. Species distribution modeling (SDM) allowed us to estimate the total range size during the Last Interglacial (LIG) and Last Glacial Maximum (LGM) as well as to indicate potential population subdivisions. Pairwise Sequentially Markovian Coalescent (PSMC) allowed us to assess fluctuations in effective population size across the same period. Additionally, we used SDM to forecast the effect of future climate change on the three species over the next 50years. We found that SDM predicts the largest range size for the cold-adapted willow grouse and rock ptarmigan during the LGM. PSMC captured intraspecific population dynamics within the last glacial period, such that the willow grouse and rock ptarmigan showed multiple bottlenecks signifying recolonization events following the termination of the LGM. We also see signals of population subdivision during the last glacial period in the black grouse, but more data are needed to strengthen this hypothesis. All three species are likely to experience range contractions under future warming, with the strongest effect on willow grouse and rock ptarmigan due to their limited potential for northward expansion. Overall, by combining these two modeling approaches, we have provided a multifaceted examination of the biogeography of these species and how they have responded to climate change in the past. These results help us understand how cold-adapted species may respond to future climate changes.

Keywords
climate change, demographic history, Pleistocene, PSMC, species distribution modelling, Tetraoninae
National Category
Ecology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-295480 (URN)10.1002/ece3.4163 (DOI)000439769400025 ()30038766 (PubMedID)
Funder
Swedish Research Council, 621-2013-5418
Note

Title in Thesis list of papers: Past and potential future dynamics of three grouse species using ecological and whole genome coalescent modelling

Available from: 2016-06-07 Created: 2016-06-07 Last updated: 2018-10-05Bibliographically approved
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