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Tusso, S., Nieuwenhuis, B. P. S., Sedlazeck, F. J., Davey, J. W., Jeffares, D. C. & Wolf, J. B. W. (2019). Ancestral admixture is the main determinant of global biodiversity in fission yeast. Molecular biology and evolution, 36(9), 1975-1989
Open this publication in new window or tab >>Ancestral admixture is the main determinant of global biodiversity in fission yeast
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2019 (English)In: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 36, no 9, p. 1975-1989Article in journal (Refereed) Published
Abstract [en]

Mutation and recombination are key evolutionary processes governing phenotypic variation and reproductive isolation. We here demonstrate that biodiversity within all globally known strains of Schizosaccharomyces pombe arose through admixture between two divergent ancestral lineages. Initial hybridization was inferred to have occurred similar to 20-60 sexual outcrossing generations ago consistent with recent, human-induced migration at the onset of intensified transcontinental trade. Species-wide heritable phenotypic variation was explained near-exclusively by strain-specific arrangements of alternating ancestry components with evidence for transgressive segregation. Reproductive compatibility between strains was likewise predicted by the degree of shared ancestry. To assess the genetic determinants of ancestry block distribution across the genome, we characterized the type, frequency, and position of structural genomic variation using nanopore and single-molecule real-time sequencing. Despite being associated with double-strand break initiation points, over 800 segregating structural variants exerted overall little influence on the introgression landscape or on reproductive compatibility between strains. In contrast, we found strong ancestry disequilibrium consistent with negative epistatic selection shaping genomic ancestry combinations during the course of hybridization. This study provides a detailed, experimentally tractable example that genomes of natural populations are mosaics reflecting different evolutionary histories. Exploiting genome-wide heterogeneity in the history of ancestral recombination and lineage-specific mutations sheds new light on the population history of S. pombe and highlights the importance of hybridization as a creative force in generating biodiversity.

Place, publisher, year, edition, pages
Oxford University Press, 2019
Keywords
hybridization, structural variation, epistasis, reproductive isolation, transgression, Schizosaccharomyces pombe
National Category
Evolutionary Biology Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-390729 (URN)10.1093/molbev/msz126 (DOI)000493043800011 ()31225876 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish National Infrastructure for Computing (SNIC)NIH (National Institute of Health), UM1 HG008898
Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-11-18Bibliographically approved
Knief, U., Bossu, C. M., Saino, N., Hansson, B., Poelstra, J., Vijay, N., . . . Wolf, J. B. W. (2019). Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone. Nature Ecology & Evolution, 3(4), 570-576
Open this publication in new window or tab >>Epistatic mutations under divergent selection govern phenotypic variation in the crow hybrid zone
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2019 (English)In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 3, no 4, p. 570-576Article in journal (Refereed) Published
Abstract [en]

The evolution of genetic barriers opposing interspecific gene flow is key to the origin of new species. Drawing from information on over 400 admixed genomes sourced from replicate transects across the European hybrid zone between all-black carrion crows and grey-coated hooded crows, we decipher the interplay between phenotypic divergence and selection at the molecular level. Over 68% of plumage variation was explained by epistasis between the gene NDP and a similar to 2.8-megabase region on chromosome 18 with suppressed recombination. Both pigmentation loci showed evidence for divergent selection resisting introgression. This study reveals how few, large-effect loci can govern prezygotic isolation and shield phenotypic divergence from gene flow.

National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-382256 (URN)10.1038/s41559-019-0847-9 (DOI)000462542100018 ()30911146 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationEU, European Research Council, ERCStG-336536 FuncSpecGen
Available from: 2019-04-23 Created: 2019-04-23 Last updated: 2019-04-23Bibliographically approved
Grosser, S., Sauer, J., Paijmans, A. J., Caspers, B. A., Forcada, J., Wolf, J. B. W. & Hoffman, J. I. (2019). Fur seal microbiota are shaped by the social and physical environment, show mother-offspring similarities and are associated with host genetic quality. Molecular Ecology, 28(9), 2406-2422
Open this publication in new window or tab >>Fur seal microbiota are shaped by the social and physical environment, show mother-offspring similarities and are associated with host genetic quality
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 9, p. 2406-2422Article in journal (Refereed) Published
Abstract [en]

Despite an increasing appreciation of the importance of host-microbe interactions in ecological and evolutionary processes, the factors shaping microbial communities in wild populations remain poorly understood. We therefore exploited a natural experiment provided by two adjacent Antarctic fur seal (Arctocephalus gazella) colonies of high and low social density and combined 16S rRNA metabarcoding with microsatellite profiling of mother-offspring pairs to investigate environmental and genetic influences on skin microbial communities. Seal-associated bacterial communities differed profoundly between the two colonies, despite the host populations themselves being genetically undifferentiated. Consistent with the hypothesis that social stress depresses bacterial diversity, we found that microbial alpha diversity was significantly lower in the high-density colony. Seals from one of the colonies that contained a stream also carried a subset of freshwater-associated bacteria, indicative of an influence of the physical environment. Furthermore, mothers and their offspring shared similar microbial communities, in support of the notion that microbes may facilitate mother-offspring recognition. Finally, a significant negative association was found between bacterial diversity and heterozygosity, a measure of host genetic quality. Our study thus reveals a complex interplay between environmental and host genetic effects, while also providing empirical support for the leash model of host control, which posits that bacterial communities are driven not only by bottom-up species interactions, but also by top-down host regulation. Taken together, our findings have broad implications for understanding host-microbe interactions as well as prokaryotic diversity in general.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
Keywords
Arctocephalus gazella, host control, inbreeding, mother-offspring recognition, pinniped, skin microbiome
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-389876 (URN)10.1111/mec.15070 (DOI)000471073000019 ()30849214 (PubMedID)
Funder
German Research Foundation (DFG)
Available from: 2019-07-31 Created: 2019-07-31 Last updated: 2019-07-31Bibliographically approved
Hooper, R., Brealey, J. C., van der Valk, T., Alberdi, A., Durban, J. W., Fearnbach, H., . . . Guschanski, K. (2019). Host-derived population genomics data provides insights into bacterial and diatom composition of the killer whale skin. Molecular Ecology, 28(2), 484-502
Open this publication in new window or tab >>Host-derived population genomics data provides insights into bacterial and diatom composition of the killer whale skin
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 2, p. 484-502Article in journal (Refereed) Published
Abstract [en]

Recent exploration into the interactions and relationship between hosts and their microbiota has revealed a connection between many aspects of the host's biology, health and associated micro-organisms. Whereas amplicon sequencing has traditionally been used to characterize the microbiome, the increasing number of published population genomics data sets offers an underexploited opportunity to study microbial profiles from the host shotgun sequencing data. Here, we use sequence data originally generated from killer whale Orcinus orca skin biopsies for population genomics, to characterize the skin microbiome and investigate how host social and geographical factors influence the microbial community composition. Having identified 845 microbial taxa from 2.4 million reads that did not map to the killer whale reference genome, we found that both ecotypic and geographical factors influence community composition of killer whale skin microbiomes. Furthermore, we uncovered key taxa that drive the microbiome community composition and showed that they are embedded in unique networks, one of which is tentatively linked to diatom presence and poor skin condition. Community composition differed between Antarctic killer whales with and without diatom coverage, suggesting that the previously reported episodic migrations of Antarctic killer whales to warmer waters associated with skin turnover may control the effects of potentially pathogenic bacteria such as Tenacibaculum dicentrarchi. Our work demonstrates the feasibility of microbiome studies from host shotgun sequencing data and highlights the importance of metagenomics in understanding the relationship between host and microbial ecology.

Place, publisher, year, edition, pages
John Wiley & Sons, 2019
Keywords
Orcinus orca, Cetacea, contamination, metagenomics, microbiota
National Category
Zoology
Identifiers
urn:nbn:se:uu:diva-374203 (URN)10.1111/mec.14860 (DOI)000459345000024 ()30187987 (PubMedID)
Funder
EU, European Research Council, ERCStG‐336536EU, Horizon 2020, 663830Swedish Research Council Formas, 2016-00835
Note

These authors contributed equally to this work: Rebecca Hooper, Jaelle C. Brealey, Katerina Guschanski, Andrew D. Foote

Available from: 2019-01-18 Created: 2019-01-18 Last updated: 2019-08-01Bibliographically approved
Wu, C.-C., Klaesson, A., Buskas, J., Ranefall, P., Mirzazadeh, R., Söderberg, O. & Wolf, J. B. W. (2019). In situ quantification of individual mRNA transcripts in melanocytes discloses gene regulation of relevance to speciation. Journal of Experimental Biology, 222(5)
Open this publication in new window or tab >>In situ quantification of individual mRNA transcripts in melanocytes discloses gene regulation of relevance to speciation
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2019 (English)In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 222, no 5Article in journal (Refereed) Published
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-381095 (URN)10.1242/jeb.194431 (DOI)000461414600021 ()30718374 (PubMedID)
Funder
EU, European Research Council, ERCStG-336536Swedish Research Council, 621-2013-4510Knut and Alice Wallenberg Foundation
Available from: 2019-03-08 Created: 2019-04-15 Last updated: 2019-05-07Bibliographically approved
Tao, Y.-T., Suo, F., Tusso, S., Wang, Y.-K., Huang, S., Wolf, J. B. W. & Du, L.-L. (2019). Intraspecific diversity of fission yeast mitochondrial genomes. Genome Biology and Evolution, 11(8), 2312-2329
Open this publication in new window or tab >>Intraspecific diversity of fission yeast mitochondrial genomes
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2019 (English)In: Genome Biology and Evolution, ISSN 1759-6653, E-ISSN 1759-6653, Vol. 11, no 8, p. 2312-2329Article in journal (Refereed) Published
Abstract [en]

The fission yeast Schizosaccharomyces pombe is an important model organism, but its natural diversity and evolutionary history remain under-studied. In particular, the population genomics of the S. pombe mitochondrial genome (mitogenome) has not been thoroughly investigated. Here, we assembled the complete circular-mapping mitogenomes of 192 S. pombe isolates de novo, and found that these mitogenomes belong to 69 nonidentical sequence types ranging from 17,618 to 26,910 bp in length. Using the assembled mitogenomes, we identified 20 errors in the reference mitogenome and discovered two previously unknown mitochondrial introns. Analyzing sequence diversity of these 69 types of mitogenomes revealed two highly distinct clades, with only three mitogenomes exhibiting signs of inter-clade recombination. This diversity pattern suggests that currently available S. pombe isolates descend from two long-separated ancestral lineages. This conclusion is corroborated by the diversity pattern of the recombination-repressed K-region located between donor mating-type loci mat2 and mat3 in the nuclear genome. We estimated that the two ancestral S. pombe lineages diverged about 31 million generations ago. These findings shed new light on the evolution of S. pombe and the data sets generated in this study will facilitate future research on genome evolution.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-390730 (URN)10.1093/gbe/evz165 (DOI)000484266300022 ()31364709 (PubMedID)
Available from: 2019-08-14 Created: 2019-08-14 Last updated: 2019-10-17Bibliographically approved
Foote, A. D., Martin, M. D., Louis, M., Pacheco, G., Robertson, K. M., Sinding, M.-H. S., . . . Morin, P. A. (2019). Killer whale genomes reveal a complex history of recurrent admixture and vicariance. Molecular Ecology, 28(14), 3427-3444
Open this publication in new window or tab >>Killer whale genomes reveal a complex history of recurrent admixture and vicariance
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2019 (English)In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 28, no 14, p. 3427-3444Article in journal (Refereed) Published
Abstract [en]

Reconstruction of the demographic and evolutionary history of populations assuming a consensus tree-like relationship can mask more complex scenarios, which are prevalent in nature. An emerging genomic toolset, which has been most comprehensively harnessed in the reconstruction of human evolutionary history, enables molecular ecologists to elucidate complex population histories. Killer whales have limited extrinsic barriers to dispersal and have radiated globally, and are therefore a good candidate model for the application of such tools. Here, we analyse a global data set of killer whale genomes in a rare attempt to elucidate global population structure in a nonhuman species. We identify a pattern of genetic homogenisation at lower latitudes and the greatest differentiation at high latitudes, even between currently sympatric lineages. The processes underlying the major axis of structure include high drift at the edge of species' range, likely associated with founder effects and allelic surfing during postglacial range expansion. Divergence between Antarctic and non-Antarctic lineages is further driven by ancestry segments with up to fourfold older coalescence time than the genome-wide average; relicts of a previous vicariance during an earlier glacial cycle. Our study further underpins that episodic gene flow is ubiquitous in natural populations, and can occur across great distances and after substantial periods of isolation between populations. Thus, understanding the evolutionary history of a species requires comprehensive geographic sampling and genome-wide data to sample the variation in ancestry within individuals.

Place, publisher, year, edition, pages
WILEY, 2019
Keywords
admixture, drift, genomics, population structure, secondary contact
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-395558 (URN)10.1111/mec.15099 (DOI)000482148400011 ()31131963 (PubMedID)
Available from: 2019-10-21 Created: 2019-10-21 Last updated: 2019-10-21Bibliographically approved
Stoffel, M. A., Humble, E., Paijmans, A. J., Acevedo-Whitehouse, K., Chilvers, B. L., Dickerson, B., . . . Hoffman, J. I. (2018). Demographic histories and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history. Nature Communications, 9, Article ID 4836.
Open this publication in new window or tab >>Demographic histories and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 4836Article in journal (Refereed) Published
Abstract [en]

A central paradigm in conservation biology is that population bottlenecks reduce genetic diversity and population viability. In an era of biodiversity loss and climate change, understanding the determinants and consequences of bottlenecks is therefore an important challenge. However, as most studies focus on single species, the multitude of potential drivers and the consequences of bottlenecks remain elusive. Here, we combined genetic data from over 11,000 individuals of 30 pinniped species with demographic, ecological and life history data to evaluate the consequences of commercial exploitation by 18th and 19th century sealers. We show that around one third of these species exhibit strong signatures of recent population declines. Bottleneck strength is associated with breeding habitat and mating system variation, and together with global abundance explains much of the variation in genetic diversity across species. Overall, bottleneck intensity is unrelated to IUCN status, although the three most heavily bottlenecked species are endangered. Our study reveals an unforeseen interplay between human exploitation, animal biology, demographic declines and genetic diversity.

Place, publisher, year, edition, pages
NATURE PUBLISHING GROUP, 2018
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-371873 (URN)10.1038/s41467-018-06695-z (DOI)000450274000001 ()30446730 (PubMedID)
Available from: 2019-01-07 Created: 2019-01-07 Last updated: 2019-01-07Bibliographically approved
Humble, E., Dasmahapatra, K. K., Martínez Barrio, Á., Gregorio, I., Forcada, J., Polikeit, A.-C., . . . Hoffman, J. I. (2018). RAD Sequencing and a Hybrid Antarctic Fur Seal Genome Assembly Reveal Rapidly Decaying Linkage Disequilibrium, Global Population Structure and Evidence for Inbreeding. G3: Genes, Genomes, Genetics, 8(8), 2709-2722
Open this publication in new window or tab >>RAD Sequencing and a Hybrid Antarctic Fur Seal Genome Assembly Reveal Rapidly Decaying Linkage Disequilibrium, Global Population Structure and Evidence for Inbreeding
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2018 (English)In: G3: Genes, Genomes, Genetics, ISSN 2160-1836, E-ISSN 2160-1836, Vol. 8, no 8, p. 2709-2722Article in journal (Refereed) Published
Abstract [en]

Recent advances in high throughput sequencing have transformed the study of wild organisms by facilitating the generation of high quality genome assemblies and dense genetic marker datasets. These resources have the potential to significantly advance our understanding of diverse phenomena at the level of species, populations and individuals, ranging from patterns of synteny through rates of linkage disequilibrium (LD) decay and population structure to individual inbreeding. Consequently, we used PacBio sequencing to refine an existing Antarctic fur seal (Arctocephalus gazella) genome assembly and genotyped 83 individuals from six populations using restriction site associated DNA (RAD) sequencing. The resulting hybrid genome comprised 6,169 scaffolds with an N50 of 6.21 Mb and provided clear evidence for the conservation of large chromosomal segments between the fur seal and dog (Canis lupus familiaris). Focusing on the most extensively sampled population of South Georgia, we found that LD decayed rapidly, reaching the background level by around 400 kb, consistent with other vertebrates but at odds with the notion that fur seals experienced a strong historical bottleneck. We also found evidence for population structuring, with four main Antarctic island groups being resolved. Finally, appreciable variance in individual inbreeding could be detected, reflecting the strong polygyny and site fidelity of the species. Overall, our study contributes important resources for future genomic studies of fur seals and other pinnipeds while also providing a clear example of how high throughput sequencing can generate diverse biological insights at multiple levels of organization.

Place, publisher, year, edition, pages
GENETICS SOCIETY AMERICA, 2018
Keywords
PacBio sequencing, RAD sequencing, comparative genomics, single nucleotide polymorphism (SNP), linkage disequilibrium (LD), population structure, genomic inbreeding coefficient
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-364921 (URN)10.1534/g3.118.200171 (DOI)000440327400017 ()29954843 (PubMedID)
Funder
Swedish Research Council Formas, 231-2012-450Knut and Alice Wallenberg FoundationNERC - the Natural Environment Research Council, NE/K012886/1
Available from: 2018-11-08 Created: 2018-11-08 Last updated: 2018-11-08Bibliographically approved
Nieuwenhuis, B. P. S., Tusso Gomez, S., Bjerling, P., Stångberg, J., Wolf, J. B. W. & Immler, S. (2018). Repeated evolution of self-compatibility for reproductive assurance. Nature Communications, 9, Article ID 1639.
Open this publication in new window or tab >>Repeated evolution of self-compatibility for reproductive assurance
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2018 (English)In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 9, article id 1639Article in journal (Refereed) Published
Abstract [en]

Sexual reproduction in eukaryotes requires the fusion of two compatible gametes of opposite sexes or mating types. To meet the challenge of finding a mating partner with compatible gametes, evolutionary mechanisms such as hermaphroditism and self-fertilization have repeatedly evolved. Here, by combining the insights from comparative genomics, computer simulations and experimental evolution in fission yeast, we shed light on the conditions promoting separate mating types or self-compatibility by mating-type switching. Analogous to multiple independent transitions between switchers and non-switchers in natural populations mediated by structural genomic changes, novel switching genotypes readily evolved under selection in the experimental populations. Detailed fitness measurements accompanied by computer simulations show the benefits and costs of switching during sexual and asexual reproduction, governing the occurrence of both strategies in nature. Our findings illuminate the trade-off between the benefits of reproductive assurance and its fitness costs under benign conditions facilitating the evolution of self-compatibility.

National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-354954 (URN)10.1038/s41467-018-04054-6 (DOI)000430674000028 ()29691402 (PubMedID)
Funder
Swedish Research CouncilEU, European Research Council, HapSelA-336633Carl Tryggers foundation
Note

These authors jointly supervised this work: Jochen B.W. Wolf, Simone Immler.

Available from: 2018-06-25 Created: 2018-06-25 Last updated: 2019-09-03Bibliographically approved
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ORCID iD: ORCID iD iconorcid.org/0000-0002-2958-5183

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