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Kawakami, Takeshi
Publications (10 of 16) Show all publications
Kawakami, T., Wallberg, A., Olsson, A., Wintermantel, D., de Miranda, J. R., Allsopp, M., . . . Webster, M. T. (2019). Substantial Heritable Variation in Recombination Rate on Multiple Scales in Honeybees and Bumblebees. Genetics, 212(4), 1101-1119
Open this publication in new window or tab >>Substantial Heritable Variation in Recombination Rate on Multiple Scales in Honeybees and Bumblebees
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2019 (English)In: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 212, no 4, p. 1101-1119Article in journal (Refereed) Published
Abstract [en]

Meiotic recombination shuffles genetic variation and promotes correct segregation of chromosomes. Rates of recombination vary on several scales, both within genomes and between individuals, and this variation is affected by both genetic and environmental factors. Social insects have extremely high rates of recombination, although the evolutionary causes of this are not known. Here, we estimate rates of crossovers and gene conversions in 22 colonies of the honeybee, Apis mellifera, and 9 colonies of the bumblebee, Bombus terrestris, using direct sequencing of 299 haploid drone offspring. We confirm that both species have extremely elevated crossover rates, with higher rates measured in the highly eusocial honeybee than the primitively social bumblebee. There are also significant differences in recombination rate between subspecies of honeybee. There is substantial variation in genome-wide recombination rate between individuals of both A. mellifera and B. terrestris and the distribution of these rates overlap between species. A large proportion of interindividual variation in recombination rate is heritable, which indicates the presence of variation in trans-acting factors that influence recombination genome-wide. We infer that levels of crossover interference are significantly lower in honeybees compared to bumblebees, which may be one mechanism that contributes to higher recombination rates in honeybees. We also find a significant increase in recombination rate with distance from the centromere, mirrored by methylation differences. We detect a strong transmission bias due to GC-biased gene conversion associated with noncrossover gene conversions. Our results shed light on the mechanistic causes of extreme rates of recombination in social insects and the genetic architecture of recombination rate variation.

Place, publisher, year, edition, pages
GENETICS SOCIETY AMERICA, 2019
Keywords
Recombination, honeybee, bumblebee, crossing over, evolution of sociality
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-393827 (URN)10.1534/genetics.119.302008 (DOI)000482224900009 ()31152071 (PubMedID)
Funder
Swedish Research Council, 2014-6325Swedish Research Council, 2014-5096Swedish Research Council, 2018-03896
Available from: 2019-10-02 Created: 2019-10-02 Last updated: 2019-10-02Bibliographically approved
Vijay, N., Weissensteiner, M., Burri, R., Kawakami, T., Ellegren, H. & Wolf, J. B. W. (2017). Genomewide patterns of variation in genetic diversity are shared among populations, species and higher-order taxa. Molecular Ecology, 26(16), 4284-4295
Open this publication in new window or tab >>Genomewide patterns of variation in genetic diversity are shared among populations, species and higher-order taxa
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2017 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 16, p. 4284-4295Article in journal (Refereed) Published
Abstract [en]

Genomewide screens of genetic variation within and between populations can reveal signatures of selection implicated in adaptation and speciation. Genomic regions with low genetic diversity and elevated differentiation reflective of locally reduced effective population sizes (N-e) are candidates for barrier loci contributing to population divergence. Yet, such candidate genomic regions need not arise as a result of selection promoting adaptation or advancing reproductive isolation. Linked selection unrelated to lineage-specific adaptation or population divergence can generate comparable signatures. It is challenging to distinguish between these processes, particularly when diverging populations share ancestral genetic variation. In this study, we took a comparative approach using population assemblages from distant clades assessing genomic parallelism of variation in N-e. Utilizing population-level polymorphism data from 444 resequenced genomes of three avian clades spanning 50 million years of evolution, we tested whether population genetic summary statistics reflecting genomewide variation in N-e would covary among populations within clades, and importantly, also among clades where lineage sorting has been completed. All statistics including population-scaled recombination rate (rho), nucleotide diversity (pi) and measures of genetic differentiation between populations (F-ST, PBS, d(xy)) were significantly correlated across all phylogenetic distances. Moreover, genomic regions with elevated levels of genetic differentiation were associated with inferred pericentromeric and subtelomeric regions. The phylogenetic stability of diversity landscapes and stable association with genomic features support a role of linked selection not necessarily associated with adaptation and speciation in shaping patterns of genomewide heterogeneity in genetic diversity.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
background selection, genetic diversity, genetic draft, genetic hitchhiking, linked selection, recombination rate, speciation genetics
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-333716 (URN)10.1111/mec.14195 (DOI)000407255100013 ()28570015 (PubMedID)
Funder
Swedish Research Council, 621-2010-5553, 2014-6325, 2013-08721EU, European Research Council, ERCStG-336536Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)
Available from: 2017-11-16 Created: 2017-11-16 Last updated: 2019-01-07Bibliographically approved
Kawakami, T., Mugal, C., Suh, A., Nater, A., Burri, R., Smeds, L. & Ellegren, H. (2017). Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds. Molecular Ecology, 26(16), 4158-4172
Open this publication in new window or tab >>Whole-genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine-scale recombination rate variation in birds
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2017 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 26, no 16, p. 4158-4172Article in journal (Refereed) Published
Abstract [en]

Recombination rate is heterogeneous across the genome of various species and so are genetic diversity and differentiation as a consequence of linked selection. However, we still lack a clear picture of the underlying mechanisms for regulating recombination. Here we estimated fine-scale population recombination rate based on the patterns of linkage disequilibrium across the genomes of multiple populations of two closely related flycatcher species (Ficedula albicollis and F. hypoleuca). This revealed an overall conservation of the recombination landscape between these species at the scale of 200 kb, but we also identified differences in the local rate of recombination despite their recent divergence (<1 million years). Genetic diversity and differentiation were associated with recombination rate in a lineage-specific manner, indicating differences in the extent of linked selection between species. We detected 400-3,085 recombination hotspots per population. Location of hotspots was conserved between species, but the intensity of hotspot activity varied between species. Recombination hotspots were primarily associated with CpG islands (CGIs), regardless of whether CGIs were at promoter regions or away from genes. Recombination hotspots were also associated with specific transposable elements (TEs), but this association appears indirect due to shared preferences of the transposition machinery and the recombination machinery for accessible open chromatin regions. Our results suggest that CGIs are a major determinant of the localization of recombination hotspots, and we propose that both the distribution of TEs and fine-scale variation in recombination rate may be associated with the evolution of the epigenetic landscape.

Place, publisher, year, edition, pages
WILEY, 2017
Keywords
CpG island, GC-biased gene conversion, linked selection, population genomics, recombination, transposon
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-333715 (URN)10.1111/mec.14197 (DOI)000407255100005 ()28597534 (PubMedID)
Funder
Swedish Research Council, 2007-8731, 2010-5650, 2013-8271, 2014-6325Knut and Alice Wallenberg Foundation
Available from: 2017-11-21 Created: 2017-11-21 Last updated: 2018-02-22Bibliographically approved
Rönnegård, L., McFarlane, S. E., Husby, A., Kawakami, T., Ellegren, H. & Qvarnström, A. (2016). Increasing the power of genome wide association studies in natural populations using repeated measures - evaluation and implementation. Methods in Ecology and Evolution, 7(7), 792-799
Open this publication in new window or tab >>Increasing the power of genome wide association studies in natural populations using repeated measures - evaluation and implementation
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2016 (English)In: Methods in Ecology and Evolution, ISSN 2041-210X, E-ISSN 2041-210X, Vol. 7, no 7, p. 792-799Article in journal (Refereed) Published
Abstract [en]

1. Genomewide association studies (GWAS) enable detailed dissections of the genetic basis for organisms' ability to adapt to a changing environment. In long-term studies of natural populations, individuals are often marked at one point in their life and then repeatedly recaptured. It is therefore essential that a method for GWAS includes the process of repeated sampling. In a GWAS, the effects of thousands of single-nucleotide polymorphisms (SNPs) need to be fitted and any model development is constrained by the computational requirements. A method is therefore required that can fit a highly hierarchical model and at the same time is computationally fast enough to be useful. 2. Our method fits fixed SNP effects in a linear mixed model that can include both random polygenic effects and permanent environmental effects. In this way, the model can correct for population structure and model repeated measures. The covariance structure of the linear mixed model is first estimated and subsequently used in a generalized least squares setting to fit the SNP effects. The method was evaluated in a simulation study based on observed genotypes from a long-term study of collared flycatchers in Sweden. 3. The method we present here was successful in estimating permanent environmental effects from simulated repeated measures data. Additionally, we found that especially for variable phenotypes having large variation between years, the repeated measurements model has a substantial increase in power compared to a model using average phenotypes as a response. 4. The method is available in the R package RepeatABEL. It increases the power in GWAS having repeated measures, especially for long-term studies of natural populations, and the R implementation is expected to facilitate modelling of longitudinal data for studies of both animal and human populations.

Keywords
Ficedula albicollis, genomic relationship, hierarchical generalized linear model, single-nucleotide polymorphisms
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-301427 (URN)10.1111/2041-210X.12535 (DOI)000379957400004 ()
Funder
EU, European Research CouncilKnut and Alice Wallenberg FoundationSwedish Research CouncilStiftelsen Olle Engkvist Byggmästare
Available from: 2016-08-23 Created: 2016-08-23 Last updated: 2018-08-10Bibliographically approved
Tetreault, H. M., Kawakami, T., Ungerer, M. C. & Levy, C. (2016). Low Temperature Tolerance in the Perennial Sunflower Helianthus maximiliani. The American midland naturalist, 175(1), 91-102
Open this publication in new window or tab >>Low Temperature Tolerance in the Perennial Sunflower Helianthus maximiliani
2016 (English)In: The American midland naturalist, ISSN 0003-0031, E-ISSN 1938-4238, Vol. 175, no 1, p. 91-102Article in journal (Refereed) Published
Abstract [en]

Species distributed across diverse climate and thermal conditions represent opportune systems for studying tolerance of low temperature stress. We examined variation in cold acclimation capacity and freezing tolerance among three natural populations (Texas, Kansas, and Manitoba) of the perennial sunflower species Helianthus maximiliani, originally collected across 2134 km in central North America. Tolerance to low temperatures was evaluated through leaf electrolyte leakage assays that quantify loss of cellular electrolytes into an aqueous medium due to plasma membrane damage. Freezing tolerance was highest for plants from the northernmost latitude (Manitoba population) under both non cold-acclimated and cold-acclimated experimental conditions. Individuals from Kansas and Texas populations exhibited lower freezing tolerance compared to Manitoba but did not differ from one another. Plants from all populations retain the ability to increase freezing tolerance through the process of cold acclimation. Freezing tolerance of Manitoba x Texas F1 hybrids was statistically indistinguishable from plants from the Texas population and possible explanations for these observations are discussed. Analysis of flowering specimens from herbaria records of corresponding regional locations indicates considerable variation in flowering phenology whereby flowering occurs progressively earlier with increasing latitude. This phenological variation may provide an additional mechanism of coping with low temperature stress through temporal avoidance.

National Category
Botany
Identifiers
urn:nbn:se:uu:diva-298920 (URN)10.1674/amid-175-01-91-102.1 (DOI)000376748900009 ()
Available from: 2016-07-12 Created: 2016-07-12 Last updated: 2017-11-28Bibliographically approved
Husby, A., Kawakami, T., Ronnegard, L., Smeds, L., Ellegren, H. & Qvarnström, A. (2015). Genome-wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life-history trait. Proceedings of the Royal Society of London. Biological Sciences, 282(1806)
Open this publication in new window or tab >>Genome-wide association mapping in a wild avian population identifies a link between genetic and phenotypic variation in a life-history trait
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2015 (English)In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 282, no 1806Article in journal (Refereed) Published
Abstract [en]

Understanding the genetic basis of traits involved in adaptation is a major challenge in evolutionary biology but remains poorly understood. Here, we use genome-wide association mapping using a custom 50 k single nucleotide polymorphism (SNP) array in a natural population of collared flycatchers to examine the genetic basis of clutch size, an important life-history trait in many animal species. We found evidence for an association on chromosome 18 where one SNP significant at the genome-wide level explained 3.9% of the phenotypic variance. We also detected two suggestive quantitative trait loci (QTLs) on chromosomes 9 and 26. Fitness differences among genotypes were generally weak and not significant, although there was some indication of a sex-by-genotype interaction for lifetime reproductive success at the suggestive QTL on chromosome 26. This implies that sexual antagonism may play a role in maintaining genetic variation at this QTL. Our findings provide candidate regions for a classic avian life-history trait that will be useful for future studies examining the molecular and cellular function of, as well as evolutionary mechanisms operating at, these loci.

Keywords
clutch size, egg production, Ficedula albicollis, fitness trait, GWAS, QTL
National Category
Evolutionary Biology Ecology
Identifiers
urn:nbn:se:uu:diva-252968 (URN)10.1098/rspb.2015.0156 (DOI)000353351000019 ()
Available from: 2015-05-20 Created: 2015-05-18 Last updated: 2018-02-22Bibliographically approved
Burri, R., Nater, A., Kawakami, T., Mugal, C. F., Ólason, P. I., Smeds, L., . . . Ellegren, H. (2015). Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers. Genome Research, 25(11), 1656-1665
Open this publication in new window or tab >>Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers
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2015 (English)In: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, no 11, p. 1656-1665Article in journal (Refereed) Published
Abstract [en]

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(XY) relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-268800 (URN)10.1101/gr.196485.115 (DOI)000364355600007 ()26355005 (PubMedID)
Funder
EU, European Research Council, AdG 249976Knut and Alice Wallenberg FoundationSwedish Research Council, 2010-5650Swedish Research Council, 80576801Swedish Research Council, 70374401Science for Life Laboratory - a national resource center for high-throughput molecular bioscience
Available from: 2015-12-09 Created: 2015-12-09 Last updated: 2018-02-22Bibliographically approved
Nater, A., Burri, R., Kawakami, T., Smeds, L. & Ellegren, H. (2015). Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data. Systematic Biology, 64(6), 1000-1017
Open this publication in new window or tab >>Resolving Evolutionary Relationships in Closely Related Species with Whole-Genome Sequencing Data
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2015 (English)In: Systematic Biology, ISSN 1063-5157, E-ISSN 1076-836X, Vol. 64, no 6, p. 1000-1017Article in journal (Refereed) Published
Abstract [en]

Using genetic data to resolve the evolutionary relationships of species is of major interest in evolutionary and systematic biology. However, reconstructing the sequence of speciation events, the so-called species tree, in closely related and potentially hybridizing species is very challenging. Processes such as incomplete lineage sorting and interspecific gene flow result in local gene genealogies that differ in their topology from the species tree, and analyses of few loci with a single sequence per species are likely to produce conflicting or even misleading results. To study these phenomena on a full phylogenomic scale, we use whole-genome sequence data from 200 individuals of four black-and-white flycatcher species with so far unresolved phylogenetic relationships to infer gene tree topologies and visualize genome-wide patterns of gene tree incongruence. Using phylogenetic analysis in nonoverlapping 10-kb windows, we show that gene tree topologies are extremely diverse and change on a very small physical scale. Moreover, we find strong evidence for gene flow among flycatcher species, with distinct patterns of reduced introgression on the Z chromosome. To resolve species relationships on the background of widespread gene tree incongruence, we used four complementary coalescent-based methods for species tree reconstruction, including complex modeling approaches that incorporate post-divergence gene flow among species. This allowed us to infer the most likely species tree with high confidence. Based on this finding, we show that regions of reduced effective population size, which have been suggested as particularly useful for species tree inference, can produce positively misleading species tree topologies. Our findings disclose the pitfalls of using loci potentially under selection as phylogenetic markers and highlight the potential of modeling approaches to disentangle species relationships in systems with large effective population sizes and post-divergence gene flow.

Keywords
Approximate Bayesian computation, demographic modeling, gene flow, gene tree, incomplete lineage sorting, introgression, phylogenomics, species tree
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-267189 (URN)10.1093/sysbio/syv045 (DOI)000363168100009 ()26187295 (PubMedID)
Funder
EU, European Research CouncilKnut and Alice Wallenberg FoundationSwedish Research Council, 2007-8731Swedish Research Council, 2010-5650Swedish Research Council, 2013-8271
Available from: 2015-11-20 Created: 2015-11-19 Last updated: 2018-02-22Bibliographically approved
Kawakami, T., Smeds, L., Backstrom, N., Husby, A., Qvarnström, A., Mugal, C. F., . . . Ellegren, H. (2014). A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution. Molecular Ecology, 23(16), 4035-4058
Open this publication in new window or tab >>A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution
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2014 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 16, p. 4035-4058Article, review/survey (Refereed) Published
Abstract [en]

Detailed linkage and recombination rate maps are necessary to use the full potential of genome sequencing and population genomic analyses. We used a custom collared flycatcher 50K SNP array to develop a high-density linkage map with 37262 markers assigned to 34 linkage groups in 33 autosomes and the Z chromosome. The best-order map contained 4215 markers, with a total distance of 3132cM and a mean genetic distance between markers of 0.12cM. Facilitated by the array being designed to include markers from most scaffolds, we obtained a second-generation assembly of the flycatcher genome that approaches full chromosome sequences (N50 super-scaffold size 20.2Mb and with 1.042Gb (of 1.116Gb) anchored to and mostly ordered and oriented along chromosomes). We found that flycatcher and zebra finch chromosomes are entirely syntenic but that inversions at mean rates of 1.5-2.0 event (6.6-7.5Mb) per My have changed the organization within chromosomes, rates high enough for inversions to potentially have been involved with many speciation events during avian evolution. The mean recombination rate was 3.1cM/Mb and correlated closely with chromosome size, from 2cM/Mb for chromosomes >100Mb to >10cM/Mb for chromosomes <10Mb. This size dependence seemed entirely due to an obligate recombination event per chromosome; if 50cM was subtracted from the genetic lengths of chromosomes, the rate per physical unit DNA was constant across chromosomes. Flycatcher recombination rate showed similar variation along chromosomes as chicken but lacked the large interior recombination deserts characteristic of zebra finch chromosomes.

Keywords
collared flycatcher, linkage map, recombination rate, SNP array
National Category
Evolutionary Biology Biochemistry and Molecular Biology Biological Sciences
Identifiers
urn:nbn:se:uu:diva-232208 (URN)10.1111/mec.12810 (DOI)000340419800010 ()
Note

Kawakami and Smeds contributed equally.

Available from: 2014-09-19 Created: 2014-09-15 Last updated: 2018-02-22Bibliographically approved
Kawakami, T., Backström, N., Burri, R., Husby, A., Ólason, P., Rice, A. M., . . . Ellegren, H. (2014). Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array. Molecular Ecology Resources, 14(6), 1248-1260
Open this publication in new window or tab >>Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single-nucleotide polymorphism array
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2014 (English)In: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 14, no 6, p. 1248-1260Article in journal (Refereed) Published
Abstract [en]

With the access to draft genome sequence assemblies and whole-genome resequencing data from population samples, molecular ecology studies will be able to take truly genome-wide approaches. This now applies to an avian model system in ecological and evolutionary research: Old World flycatchers of the genus Ficedula, for which we recently obtained a 1.1Gb collared flycatcher genome assembly and identified 13 million single-nucleotide polymorphism (SNP)s in population resequencing of this species and its sister species, pied flycatcher. Here, we developed a custom 50K Illumina iSelect flycatcher SNP array with markers covering 30 autosomes and the Z chromosome. Using a number of selection criteria for inclusion in the array, both genotyping success rate and polymorphism information content (mean marker heterozygosity=0.41) were high. We used the array to assess linkage disequilibrium (LD) and hybridization in flycatchers. Linkage disequilibrium declined quickly to the background level at an average distance of 17kb, but the extent of LD varied markedly within the genome and was more than 10-fold higher in genomic islands' of differentiation than in the rest of the genome. Genetic ancestry analysis identified 33 F-1 hybrids but no later-generation hybrids from sympatric populations of collared flycatchers and pied flycatchers, contradicting earlier reports of backcrosses identified from much fewer number of markers. With an estimated divergence time as recently as <1Ma, this suggests strong selection against F-1 hybrids and unusually rapid evolution of reproductive incompatibility in an avian system.

Keywords
collared flycatcher, GWAS, Hybridization, pied flycatcher, single-nucleotide polymorphism genotyping, speciation
National Category
Biochemistry and Molecular Biology Ecology
Identifiers
urn:nbn:se:uu:diva-237291 (URN)10.1111/1755-0998.12270 (DOI)000343805400014 ()24784959 (PubMedID)
Available from: 2014-12-03 Created: 2014-12-01 Last updated: 2018-02-22Bibliographically approved
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