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  • 1.
    Adolfsson, Sofia
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Lack of Dosage Compensation Accompanies the Arrested Stage of Sex Chromosome Evolution in Ostriches2013Ingår i: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 30, nr 4, s. 806-810Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Sex chromosome evolution is usually seen as a process that, once initiated, will inevitably progress toward an advanced stage of degeneration of the nonrecombining chromosome. However, despite evidence that avian sex chromosome evolution was initiated > 100 Ma, ratite birds have been trapped in an arrested stage of sex chromosome divergence. We performed RNA sequencing of several tissues from male and female ostriches and assembled the transcriptome de novo. A total of 315 Z-linked genes fell into two categories: those that have equal expression level in the two sexes (for which Z-W recombination still occurs) and those that have a 2-fold excess of male expression (for which Z-W recombination has ceased). We suggest that failure to evolve dosage compensation has constrained sex chromosome divergence in this basal avian lineage. Our results indicate that dosage compensation is a prerequisite for, not only a consequence of, sex chromosome evolution.

  • 2.
    Ahlbäck Öberg, Shirin
    et al.
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet, Samhällsvetenskapliga fakulteten, Statsvetenskapliga institutionen.
    Bennich-Björkman, Li
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Karlsson, Christer
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet, Samhällsvetenskapliga fakulteten, Statsvetenskapliga institutionen.
    Lindegren, Jan
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet, Historisk-filosofiska fakulteten, Historiska institutionen.
    Widmalm, Sten
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet, Samhällsvetenskapliga fakulteten, Statsvetenskapliga institutionen.
    Widmalm, Sven
    Uppsala universitet, Humanistisk-samhällsvetenskapliga vetenskapsområdet, Historisk-filosofiska fakulteten, Institutionen för idé- och lärdomshistoria.
    Om universitetet blir aktiebolag2013Övrigt (Övrig (populärvetenskap, debatt, mm))
  • 3.
    Anderung, Cecilia
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Persson, P
    Carretero, J. M.
    Ortega, A. I.
    Arasuaga, J. L.
    Elburg, R.
    Smith, C.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Götherström, Anders
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Genetics of Iberian Bronze Age cattle remains indicate prehistoric contacts over the Strait of Gibraltar.2005Ingår i: Proceedings of the National Academy of Sciences USA, nr 102, s. 8431-8435Artikel i tidskrift (Refereegranskat)
  • 4.
    Axelsson, Erik
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolutionsbiologi. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolutionsbiologi. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Quantification of Adaptive Evolution of Genes Expressed in Avian Brain and the Population Size Effect on the Efficacy of Selection2009Ingår i: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 26, nr 5, s. 1073-1079Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Whether protein evolution is mainly due to fixation of beneficial alleles by positive selection or to random genetic drift has remained a contentious issue over the years. Here, we use two genomewide polymorphism data sets collected from chicken populations, together with divergence data from >5,000 chicken-zebra finch gene orthologs expressed in brain, to assess the amount of adaptive evolution in protein-coding genes of birds. First, we show that estimates of the fixation index (FI, the ratio of fixed nonsynonymous-to-synonymous changes over the ratio of the corresponding polymorphisms) are highly dependent on the character of the underlying data sets. Second, by using polymorphism data from high-frequency alleles, to avoid the confounding effect of slightly deleterious mutations segregating at low frequency, we estimate that about 20% of amino acid changes have been brought to fixation through positive selection during avian evolution. This estimate is intermediate to that obtained in humans (lower) and flies as well as bacteria (higher), and is consistent with population genetics theory that stipulates a positive relationship between the efficiency of selection and the effective population size. Further, by comparing the FIs for common and all alleles, we estimate that approximate to 20% of nonsynonymous variation segregating in chicken populations represent slightly deleterious mutations, which is less than in Drosophila. Overall, these results highlight the link between the effective population size and positive as well as negative selection.

  • 5.
    Axelsson, Erik
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Hultin-Rosenberg, Lina
    Brandström, Mikael
    Zwalen, Martin
    Clayton, David F.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Natural selection in protein-coding genes expressed in avian brain2008Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 17, nr 12, s. 3008-3017Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The evolution of birds from theropod dinosaurs took place approximately 150 million years ago, and was associated with a number of specific adaptations that are still evident among extant birds, including feathers, song and extravagant secondary sexual characteristics. Knowledge about the molecular evolutionary background to such adaptations is lacking. Here, we analyse the evolution of > 5000 protein-coding gene sequences expressed in zebra finch brain by comparison to orthologous sequences in chicken. Mean d(N)/d(S) is 0.085 and genes with their maximal expression in the eye and central nervous system have the lowest mean d(N)/d(S) value, while those expressed in digestive and reproductive tissues exhibit the highest. We find that fast-evolving genes (those which have higher than expected rate of nonsynonymous substitution, indicative of adaptive evolution) are enriched for biological functions such as fertilization, muscle contraction, defence response, response to stress, wounding and endogenous stimulus, and cell death. After alignment to mammalian orthologues, we identify a catalogue of 228 genes that show a significantly higher rate of protein evolution in the two bird lineages than in mammals. These accelerated bird genes, representing candidates for avian-specific adaptations, include genes implicated in vocal learning and other cognitive processes. Moreover, colouration genes evolve faster in birds than in mammals, which may have been driven by sexual selection for extravagant plumage characteristics.

  • 6.
    Axelsson, Erik
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Webster, Matthew T
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Smith, Nick G C
    Burt, David W
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Comparison of the chicken and turkey genomes reveals a higher rate of nucleotide divergence on microchromosomes than macrochromosomes.2005Ingår i: Genome Res, ISSN 1088-9051, Vol. 15, nr 1, s. 120-5Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    A distinctive feature of the avian genome is the large heterogeneity in the size of chromosomes, which are usually classified into a small number of macrochromosomes and numerous microchromosomes. These chromosome classes show characteristic differences in a number of interrelated features that could potentially affect the rate of sequence evolution, such as GC content, gene density, and recombination rate. We studied the effects of these factors by analyzing patterns of nucleotide substitution in two sets of chicken-turkey sequence alignments. First, in a set of 67 orthologous introns, divergence was significantly higher in microchromosomes (chromosomes 11-38; 11.7% divergence) than in both macrochromosomes (chromosomes 1-5; 9.9% divergence; P = 0.016) and intermediate-sized chromosomes (chromosomes 6-10; 9.5% divergence; P = 0.026). At least part of this difference was due to the higher incidence of CpG sites on microchromosomes. Second, using 155 orthologous coding sequences we noted a similar pattern, in which synonymous substitution rates on microchromosomes (13.1%) were significantly higher than were rates on macrochromosomes (10.3%; P = 0.024). Broadly assuming neutrality of introns and synonymous sites, or constraints on such sequences do not differ between chromosomal classes, these observations imply that microchromosomal genes are exposed to more germ line mutations than those on other chromosomes. We also find that dN/dS ratios for genes located on microchromosomes (average, 0.094) are significantly lower than those of macrochromosomes (average, 0.185; P = 0.025), suggesting that the proteins of genes on microchromosomes are under greater evolutionary constraint.

  • 7.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Brandström, Mikael
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Gustafsson, Lars
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och evolution, Zooekologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och evolution, Zooekologi.
    Cheng, Hans
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): Conserved synteny but gene order rearrangements on the avian Z chromosome2006Ingår i: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 174, nr 1, s. 377-386Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Data from completely sequenced genomes are likely to open the way for novel studies of the genetics of nonmodel organisms, in particular when it comes to the identification and analysis of genes responsible for traits that are under selection in natural populations. Here we use the draft sequence of the chicken genome as a starting point for linkage mapping in a wild bird species, the collared flycatcher-one of the most well-studied avian species in ecological and evolutionary research. A pedigree of 365 flycatchers was established and genotyped for single nucleotide polymorphisms in 23 genes selected from (and spread over most of) the chicken Z chromosome. All genes were also found to be located on the Z chromosome in the collared flycatcher, confirming conserved synteny at the level of gene content across distantly related avian lineages. This high degree of conservation mimics the situation seen for the mammalian X chromosome and may thus be a general feature in sex chromosome evolution, irrespective of whether there is male or female heterogamety. Alternatively, such unprecedented chromosomal conservation may be characteristic of most chromosomes in avian genome evolution. However, several internal rearrangements were observed, meaning that the transfer of map information from chicken to nonmodel bird species cannot always assume conserved gene orders. Interestingly, the rate of recombination on the Z chromosome of collared flycatchers was only similar to 50% that of chicken, challenging the widely held view that birds generally have high recombination rates.

  • 8.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Ceplitis, Helene
    Berlin, Sofia
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Gene conversion drives the evolution of HINTW, an ampliconic gene on the female-specific avian W chromosome.2005Ingår i: Mol Biol Evol, ISSN 0737-4038, Vol. 22, nr 10, s. 1992-9Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The HINTW gene on the female-specific W chromosome of chicken and other birds is amplified and present in numerous copies. Moreover, as HINTW is distinctly different from its homolog on the Z chromosome (HINTZ), is a candidate gene in avian sex determination, and evolves rapidly under positive selection, it shows several common features to ampliconic and testis-specific genes on the mammalian Y chromosome. A phylogenetic analysis within galliform birds (chicken, turkey, quail, and pheasant) shows that individual HINTW copies within each species are more similar to each other than to gene copies of related species. Such convergent evolution is most easily explained by recurrent events of gene conversion, the rate of which we estimated at 10(-6)-10(-5) per site and generation. A significantly higher GC content of HINTW than of other W-linked genes is consistent with biased gene conversion increasing the fixation probability of mutations involving G and C nucleotides. Furthermore, and as a likely consequence, the neutral substitution rate is almost twice as high in HINTW as in other W-linked genes. The region on W encompassing the HINTW gene cluster is not covered in the initial assembly of the chicken genome, but analysis of raw sequence reads indicates that gene copy number is significantly higher than a previous estimate of 40. While sexual selection is one of several factors that potentially affect the evolution of ampliconic, male-specific genes on the mammalian Y chromosome, data from HINTW provide evidence that gene amplification followed by gene conversion can evolve in female-specific chromosomes in the absence of sexual selection. The presence of multiple and highly similar copies of HINTW may be related to protein function, but, more generally, amplification and conversion offers a means to the avoidance of accumulation of deleterious mutations in nonrecombining chromosomes.

  • 9.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Fagerberg, Sofie
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome2008Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 17, nr 4, s. 964-980Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Although there is growing interest to take genomics into the complex realms of natural populations, there is a general shortage of genomic resources and tools available for wild species. This applies not at least to birds, for which genomic approaches should be helpful to questions such as adaptation, speciation and population genetics. In this study, we describe a genome-wide reference set of conserved avian gene markers, broadly applicable across birds. By aligning protein-coding sequences from the recently assembled chicken genome with orthologous sequences in zebra finch, we identified particularly conserved exonic regions flanking introns of suitable size for subsequent amplification and sequencing. Primers were designed for 242 gene markers evenly distributed across the chicken genome, with a mean inter-marker interval of 4.2 Mb. Between 78% and 93% of the markers amplified a specific product in five species tested (chicken, peregrine falcon, collared flycatcher, great reed warbler and blue tit). Two hundred markers were sequenced in collared flycatcher, yielding a total of 122.41 kb of genomic DNA sequence (12096 bp coding sequence and 110 314 bp noncoding). Intron size of collared flycatcher and chicken was highly correlated, as was GC content. A polymorphism screening using these markers in a panel of 10 unrelated collared flycatchers identified 871 single nucleotide polymorphisms (pi = 0.0029) and 33 indels (mainly very short). Avian genome characteristics such as uniform genome size and low rate of syntenic rearrangements suggest that this marker set will find broad utility as a genome-wide reference resource for molecular ecological and population genomic analysis of birds. We envision that it will be particularly useful for obtaining large-scale orthologous targets in different species--important in, for instance, phylogenetics--and for large-scale identification of evenly distributed single nucleotide polymorphisms needed in linkage mapping or in studies of gene flow and hybridization.

  • 10.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Forstmeier, Wolfgang
    Schielzeth, Holger
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mellenius, Harriet
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nam, Kiwoong
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Bolund, Elisabeth
    Webster, Matthew T.
    Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinsk biokemi och mikrobiologi. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Öst, Torbjörn
    Uppsala universitet, Medicinska och farmaceutiska vetenskapsområdet, Medicinska fakulteten, Institutionen för medicinska vetenskaper.
    Schneider, Melanie
    Kempenaers, Bart
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    The recombination landscape of the zebra finch Taeniopygia guttata genome2010Ingår i: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 20, nr 4, s. 485-495Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Understanding the causes and consequences of variation in the rate of recombination is essential since this parameter is considered to affect levels of genetic variability, the efficacy of selection, and the design of association and linkage mapping studies. However, there is limited knowledge about the factors governing recombination rate variation. We genotyped 1920 single nucleotide polymorphisms in a multigeneration pedigree of more than 1000 zebra finches (Taeniopygia guttata) to develop a genetic linkage map, and then we used these map data together with the recently available draft genome sequence of the zebra finch to estimate recombination rates in 1 Mb intervals across the genome. The average zebra finch recombination rate (1.5 cM/Mb) is higher than in humans, but significantly lower than in chicken. The local rates of recombination in chicken and zebra finch were only weakly correlated, demonstrating evolutionary turnover of the recombination landscape in birds. The distribution of recombination events was heavily biased toward ends of chromosomes, with a stronger telomere effect than so far seen in any organism. In fact, the recombination rate was as low as 0.1 cM/Mb in intervals up to 100 Mb long in the middle of the larger chromosomes. We found a positive correlation between recombination rate and GC content, as well as GC-rich sequence motifs. Levels of linkage disequilibrium (LD) were significantly higher in regions of low recombination, showing that heterogeneity in recombination rates have left a footprint on the genomic landscape of LD in zebra finch populations.

  • 11.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Karaiskou, Nikoletta
    Leder, Erica H.
    Gustafsson, Lars
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Primmer, Craig R.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    A Gene-Based Genetic Linkage Map of the Collared Flycatcher (Ficedula albicollis) Reveals Extensive Synteny and Gene-Order Conservation During 100 Million Years of Avian Evolution2008Ingår i: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 179, s. 1479-1495Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    By taking advantage of a recently developed reference markerset for avian genome analysis we have constructed a gene-basedgenetic map of the collared flycatcher, an important "ecologicalmodel" for studies of life-history evolution, sexual selection,speciation, and quantitative genetics. A pedigree of 322 birdsfrom a natural population was genotyped for 384 single nucleotidepolymorphisms (SNPs) from 170 protein-coding genes and 71 microsatellites.Altogether, 147 gene markers and 64 microsatellites form 33linkage groups with a total genetic distance of 1787 cM. Malerecombination rates are, on average, 22% higher than femalerates (total distance 1982 vs. 1627 cM). The ability to anchorthe collared flycatcher map with the chicken genome via thegene-based SNPs revealed an extraordinary degree of both syntenyand gene-order conservation during avian evolution. The greatmajority of chicken chromosomes correspond to a single linkagegroup in collared flycatchers, with only a few cases of inter-and intrachromosomal rearrangements. The rate of chromosomaldiversification, fissions/fusions, and inversions combined isthus considerably lower in birds (0.05/MY) than in mammals (0.6–2.0/MY).A dearth of repeat elements, known to promote chromosomal breakage,in avian genomes may contribute to their stability. The degreeof genome stability is likely to have important consequencesfor general evolutionary patterns and may explain, for example,the comparatively slow rate by which genetic incompatibilityamong lineages of birds evolves.

  • 12.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Lindell, Johan
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Zhang, Yu
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Palkopoulou, Eleftheria
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Sætre, Glenn-Peter
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    A high-density scan of the Z chromosome in ficedula flycatchers reveals candidate loci for diversifying selection2010Ingår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 64, nr 12, s. 3461-3475Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Theoretical and empirical data suggest that genes located on sex chromosomes may play an important role both for sexually selected traits and for traits involved in the build-up of hybrid incompatibilities. We investigated patterns of genetic variation in 73 genes located on the Z chromosomes of two species of the flycatcher genus Ficedula, the pied flycatcher and the collared flycatcher. Sequence data were evaluated for signs of selection potentially related to genomic differentiation in these young sister species, which hybridize despite reduced fitness of hybrids. Seven loci were significantly more divergent between the two species than expected under neutrality and they also displayed reduced nucleotide diversity, consistent with having been influenced by directional selection. Two of the detected candidate regions contain genes that are associated with plumage coloration in birds. Plumage characteristics play an important role in species recognition in these flycatchers suggesting that the detected genes may have been involved in the evolution of sexual isolation between the species.

  • 13.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Palkopoulou, Eleftheria
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    No evidence for Z-chromosome rearrangements between the pied flycatcher and the collared flycatcher as judged by gene-based comparative genetic maps2010Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 19, nr 16, s. 3394-3405Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Revealing the genetic basis of reproductive isolation is fundamental for understanding the speciation process. Chromosome speciation models propose a role for chromosomal rearrangements in promoting the build up of reproductive isolation between diverging populations and empirical data from several animal and plant taxa support these models. The pied flycatcher and the collared flycatcher are two closely related species that probably evolved reproductive isolation during geographical separation in Pleistocene glaciation refugia. Despite the short divergence time and current hybridization, these two species demonstrate a high degree of intrinsic post-zygotic isolation and previous studies have shown that traits involved in mate choice and hybrid viability map to the Z-chromosome. Could rearrangements of the Z-chromosome between the species explain their reproductive isolation? We developed high coverage Z-chromosome linkage maps for both species, using gene-based markers and large-scale SNP genotyping. Best order maps contained 57-62 gene markers with an estimated average density of one every 1-1.5 Mb. We estimated the recombination rates in flycatcher Z-chromosomes to 1.1-1.3 cM/Mb. A comparison of the maps of the two species revealed extensive co-linearity with no strong evidence for chromosomal rearrangements. This study does therefore not provide support the idea that sex chromosome rearrangements have caused the relatively strong post-zygotic reproductive isolation between these two Ficedula species.

  • 14.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Gustafsson, Lars
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Levels of linkage disequilibrium in a wild bird population2006Ingår i: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 2, nr 3, s. 435-438Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Population-based mapping approaches are attractive for tracing the genetic background to phenotypic traits in wild species, given that it is often difficult to gather extensive and well-defined pedigrees needed for quantitative trait locus analysis. However, the feasibility of association or hitch-hiking mapping is dependent on the degree of linkage disequilibrium. (LD) in the population, on which there is yet limited information for wild species. Here we use single nucleotide polymorphism (SNP) markers from 23 genes in a recently established linkage map of the Z chromosome of the collared flycatcher, to study the extent of LD in a natural bird population. In most but not all cases we find SNPs within the same intron (less than 500 bp) to be in perfect LD. However, LD then decays to background level at a distance 1 cM or 400-500 kb. Although LD seems more extensive than in other species, if the observed pattern is representative for other regions of the genome and turns out to be a general feature of natural bird populations, dense marker maps might be needed for genome scans aimed at identifying association between marker and trait loci.

  • 15.
    Backström, Niclas
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Saetre, Glenn-Peter
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Inferring the demographic history of European Ficedula flycatcher populations2013Ingår i: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 13, s. 2-Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Background: Inference of population and species histories and population stratification using genetic data is important for discriminating between different speciation scenarios and for correct interpretation of genome scans for signs of adaptive evolution and trait association. Here we use data from 24 intronic loci re-sequenced in population samples of two closely related species, the pied flycatcher and the collared flycatcher. Results: We applied Isolation-Migration models, assignment analyses and estimated the genetic differentiation and diversity between species and between populations within species. The data indicate a divergence time between the species of <1 million years, significantly shorter than previous estimates using mtDNA, point to a scenario with unidirectional gene-flow from the pied flycatcher into the collared flycatcher and imply that barriers to hybridisation are still permeable in a recently established hybrid zone. Furthermore, we detect significant population stratification, predominantly between the Spanish population and other pied flycatcher populations. Conclusions: Our results provide further evidence for a divergence process where different genomic regions may be at different stages of speciation. We also conclude that forthcoming analyses of genotype-phenotype relations in these ecological model species should be designed to take population stratification into account.

  • 16.
    Berggren, Karin
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Ellegren, H
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Hewitt, G M
    Seddon, J M
    Understanding the phylogeographic patterns of European hedgehogs, Erinaceus concolor and E. europaeus using the MHC.2005Ingår i: Heredity, ISSN 0018-067X, Vol. 95, nr 1, s. 84-90Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The genome of the European hedgehog, Erinaceus concolor and E. europaeus, shows a strong signal of cycles of restriction to glacial refugia and postglacial expansion. Patterns of expansion, however, differ for mitochondrial DNA (mtDNA) and preliminary analysis of nuclear markers. In this study, we determine phylogeographic patterns in the hedgehog using two loci of the major histocompatibility complex (MHC), isolated for the first time in hedgehogs. These genes show long persistence times and high polymorphism in many species because of the actions of balancing selection. Among 84 individuals screened for variation, only two DQA alleles were identified in each species, but 10 DQB alleles were found in E. concolor and six in E. europaeus. A strong effect of demography on patterns of DQB variability is observed, with only weak evidence of balancing selection. While data from mtDNA clearly subdivide both species into monophyletic subgroups, the MHC data delineate only E. concolor into distinct subgroups, supporting the preliminary findings of other nuclear markers. Together with differences in variability, this suggests that the refugia history and/or expansion patterns of E. concolor and E. europaeus differ.

  • 17.
    Berggren, Karin
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Hewitt, G. M.
    Seddon, J. M.
    Demographic effects have been more important than selection in shaping patterns of variation at MHC genes in European hedgehogs, Erinaceus europaeus and Erinaceus concolor.2005Ingår i: Heredity, nr 85, s. 84-90Artikel i tidskrift (Refereegranskat)
  • 18.
    Berlin, Sofia
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Evolutionsbiologi.
    Brandström, Mikael
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Evolutionsbiologi.
    Backström, Niclas
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Evolutionsbiologi.
    Axelsson, Erik
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Evolutionsbiologi.
    Smith, Nick G C
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Evolutionsbiologi.
    Substitution rate heterogeneity and the male mutation bias.2006Ingår i: Journal of Molecular Evolution, ISSN 0022-2844, Vol. 62, nr 2, s. 226-33Artikel i tidskrift (Refereegranskat)
  • 19.
    Berlin, Sofia
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Fast accumulation of nonsynonymous mutations on the female-specific W chromosome in birds.2006Ingår i: Journal of Molecular Evolution, ISSN 0022-2844, Vol. 62, nr 1, s. 66-72Artikel i tidskrift (Refereegranskat)
  • 20.
    Bischof, Richard
    et al.
    Norwegian Univ Life Sci, Dept Ecol & Nat Resource Management, Hogskoleveien 12, N-1430 As, Norway..
    Gregersen, Espen R.
    Norwegian Univ Life Sci, Dept Ecol & Nat Resource Management, Hogskoleveien 12, N-1430 As, Norway..
    Broseth, Henrik
    Norwegian Inst Nat Res, Tungasletta 2, N-7004 Trondheim, Norway..
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Flagstad, Oystein
    Norwegian Inst Nat Res, Tungasletta 2, N-7004 Trondheim, Norway..
    Noninvasive genetic sampling reveals intrasex territoriality in wolverines2016Ingår i: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 6, nr 5, s. 1527-1536Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Due to its conspicuous manifestations and its capacity to shape the configuration and dynamics of wild populations, territorial behavior has long intrigued ecologists. Territoriality and other animal interactions in situ have traditionally been studied via direct observations and telemetry. Here, we explore whether noninvasive genetic sampling, which is increasingly supplementing traditional field methods in ecological research, can reveal territorial behavior in an elusive carnivore, the wolverine (Gulo gulo). Using the locations of genotyped wolverine scat samples collected annually over a period of 12 years in central Norway, we test three predictions: (1) male home ranges constructed from noninvasive genetic sampling data are larger than those of females, (2) individuals avoid areas used by other conspecifics of the same sex (intrasexual territoriality), and (3) avoidance of same-sex territories diminishes or disappears after the territory owner's death. Each of these predictions is substantiated by our results: sex-specific differences in home range size and intrasexual territoriality in wolverine are patently reflected in the spatial and temporal configuration of noninvasively collected genetic samples. Our study confirms that wildlife monitoring programs can utilize the spatial information in noninvasive genetic sampling data to detect and quantify home ranges and social organization.

  • 21.
    Bolivar, Paulina
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Gueguen, Laurent
    Univ Claude Bernard Lyon 1, CNRS, UMR 5558, Lab Biol & Biometrie Evolut, Lyon, France.
    Duret, Laurent
    Univ Claude Bernard Lyon 1, CNRS, UMR 5558, Lab Biol & Biometrie Evolut, Lyon, France.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    GC-biased gene conversion conceals the prediction of the nearly neutral theory in avian genomes2019Ingår i: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 20, artikel-id 5Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Background: The nearly neutral theory of molecular evolution predicts that the efficacy of natural selection increases with the effective population size. This prediction has been verified by independent observations in diverse taxa, which show that life-history traits are strongly correlated with measures of the efficacy of selection, such as the d(N)/d(S) ratio. Surprisingly, avian taxa are an exception to this theory because correlations between life-history traits and d(N)/d(S) are apparently absent. Here we explore the role of GC-biased gene conversion on estimates of substitution rates as a potential driver of these unexpected observations.

    Results: We analyze the relationship between d(N)/d(S) estimated from alignments of 47 avian genomes and several proxies for effective population size. To distinguish the impact of GC-biased gene conversion from selection, we use an approach that accounts for non-stationary base composition and estimate d(N)/d(S) separately for changes affected or unaffected by GC-biased gene conversion. This analysis shows that the impact of GC-biased gene conversion on substitution rates can explain the lack of correlations between life-history traits and d(N)/d(S). Strong correlations between life-history traits and d(N)/d(S) are recovered after accounting for GC-biased gene conversion. The correlations are robust to variation in base composition and genomic location.

    Conclusions: Our study shows that gene sequence evolution across a wide range of avian lineages meets the prediction of the nearly neutral theory,the efficacy of selection increases with effective population size. Moreover, our study illustrates that accounting for GC-biased gene conversion is important to correctly estimate the strength of selection.

  • 22.
    Bolivar, Paulina
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Sebastiano, Matteo Rossi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Ludwig Maximilians Univ Munchen, Fac Biol, Dept Biol 2, Planegg Martinsried, Germany.
    Nater, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Univ Konstanz, Dept Biol, Chair Zool & Evolutionary Biol, Constance, Germany.
    Wang, Mi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Dutoit, Ludovic
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Biased Inference of Selection Due to GC-Biased Gene Conversion and the Rate of Protein Evolution in Flycatchers When Accounting for It2018Ingår i: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 35, nr 10, s. 2475-2486Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The rate of recombination impacts on rates of protein evolution for at least two reasons: it affects the efficacy of selection due to linkage and influences sequence evolution through the process of GC-biased gene conversion (gBGC). We studied how recombination, via gBGC, affects inferences of selection in gene sequences using comparative genomic and population genomic data from the collared flycatcher (Ficedula albicollis). We separately analyzed different mutation categories ("strong"-to-"weak" "weak-to-strong," and GC-conservative changes) and found that gBGC impacts on the distribution of fitness effects of new mutations, and leads to that the rate of adaptive evolution and the proportion of adaptive mutations among nonsynonymous substitutions are underestimated by 22-33%. It also biases inferences of demographic history based on the site frequency spectrum. In light of this impact, we suggest that inferences of selection (and demography) in lineages with pronounced gBGC should be based on GC-conservative changes only. Doing so, we estimate that 10% of nonsynonymous mutations are effectively neutral and that 27% of nonsynonymous substitutions have been fixed by positive selection in the flycatcher lineage. We also find that gene expression level, sex-bias in expression, and the number of protein-protein interactions, but not Hill-Robertson interference (HRI), are strong determinants of selective constraint and rate of adaptation of collared flycatcher genes. This study therefore illustrates the importance of disentangling the effects of different evolutionary forces and genetic factors in interpretation of sequence data, and from that infer the role of natural selection in DNA sequence evolution.

  • 23.
    Bolívar, Paulina
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina F
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nater, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Recombination Rate Variation Modulates Gene Sequence Evolution Mainly via GC-Biased Gene Conversion, Not Hill-Robertson Interference, in an Avian System2016Ingår i: Molecular biology and evolution, ISSN 0737-4038, E-ISSN 1537-1719, Vol. 33, nr 1, s. 216-227Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The ratio of nonsynonymous to synonymous substitution rates (ω) is often used to measure the strength of natural selection. However, ω may be influenced by linkage among different targets of selection, that is, Hill-Robertson interference (HRI), which reduces the efficacy of selection. Recombination modulates the extent of HRI but may also affect ω by means of GC-biased gene conversion (gBGC), a process leading to a preferential fixation of G:C ("strong," S) over A:T ("weak," W) alleles. As HRI and gBGC can have opposing effects on ω, it is essential to understand their relative impact to make proper inferences of ω. We used a model that separately estimated S-to-S, S-to-W, W-to-S, and W-to-W substitution rates in 8,423 avian genes in the Ficedula flycatcher lineage. We found that the W-to-S substitution rate was positively, and the S-to-W rate negatively, correlated with recombination rate, in accordance with gBGC but not predicted by HRI. The W-to-S rate further showed the strongest impact on both dN and dS. However, since the effects were stronger at 4-fold than at 0-fold degenerated sites, likely because the GC content of these sites is farther away from its equilibrium, ω slightly decreases with increasing recombination rate, which could falsely be interpreted as a consequence of HRI. We corroborated this hypothesis analytically and demonstrate that under particular conditions, ω can decrease with increasing recombination rate. Analyses of the site-frequency spectrum showed that W-to-S mutations were skewed toward high, and S-to-W mutations toward low, frequencies, consistent with a prevalent gBGC-driven fixation bias.

  • 24.
    Brandström, Miakel
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Genome-wide analysis of microsatellite polymorphism in chicken circumventing the ascertainment bias2008Ingår i: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 18, nr 6, s. 881-887Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Studies of microsatellites evolution based on marker data almost inherently suffer from an ascertainment bias because there is selection for the most mutable and polymorphic loci during marker development. To circumvent this bias we took advantage of whole-genome shotgun sequence data from three unrelated chicken individuals that, when aligned to the genome reference sequence, give sequence information on two chromosomes from about one-fourth (375,000) of all microsatellite loci containing di- through pentanucleotide repeat motifs in the chicken genome. Polymorphism is seen at loci with as few as five repeat units, and the proportion of dimorphic loci then increases to 50% for sequences with similar to 10 repeat units, to reach a maximum of 75%-80% for sequences with 15 or more repeat units. For any given repeat length, polymorphism increases with decreasing GC content of repeat motifs for dinucleotides, nonhairpin-forming trinucleotides, and tetranucleotides. For trinucleotide repeats which are likely to form hairpin structures, polymorphism increases with increasing GC content, indicating that the relative stability of hairpins affects the rate of replication slippage. For any given repeat length, polymorphism is significantly lower for imperfect compared to perfect repeats and repeat interruptions occur in >15% of loci. However, interruptions are not randomly distributed within repeat arrays but are preferentially located toward the ends. There is negative correlation between microsatellite abundance and single nucleotide polymorphism ( SNP) density, providing large-scale genomic support for the hypothesis that equilibrium microsatellite distributions are governed by a balance between rate of replication slippage and rate of point mutation.

  • 25.
    Brandström, Mikael
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    The genomic landscape of short insertion and deletion polymorphisms in the chicken (Gallus gallus) genome: A high frequency of deletions in tandem duplicates2007Ingår i: Genetics, ISSN 0016-6731, E-ISSN 1943-2631, Vol. 176, nr 3, s. 1691-1701Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    It is increasingly recognized that insertions and deletions(indels) are an important source of genetic as well as phenotypicdivergence and diversity. We analyzed length polymorphisms identifiedthrough partial (0.25x) shotgun sequencing of three breeds ofdomestic chicken made by the International Chicken PolymorphismMap Consortium. A data set of 140,484 short indel polymorphismsin unique DNA was identified after filtering for microsatellitestructures. There was a significant excess of tandem duplicatesat indel sites, with deletions of a duplicate motif outnumberingthe generation of duplicates through insertion. Indel densitywas lower in microchromosomes than in macrochromosomes, in theZ chromosome than in autosomes, and in 100 bp of upstream sequence,5'-UTR, and first introns than in intergenic DNA and in otherintrons. Indel density was highly correlated with single nucleotidepolymorphism (SNP) density. The mean density of indels in pairwisesequence comparisons was 1.9 x 10–4 indel events/bp, 5%the density of SNPs segregating in the chicken genome. The greatmajority of indels involved a limited number of nucleotides(median 1 bp), with A-rich motifs being overrepresented at indelsites. The overrepresentation of deletions at tandem duplicatesindicates that replication slippage in duplicate sequences isa common mechanism behind indel mutation. The correlation betweenindel and SNP density indicates common effects of mutation and/orselection on the occurrence of indels and point mutations.

  • 26. Broseth, Henrik
    et al.
    Flagstad, Oystein
    Wärdig, Cecilia
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Johansson, Malin
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Large-scale noninvasive genetic monitoring of wolverines using scats reveals density dependent adult survival2010Ingår i: Biological Conservation, ISSN 0006-3207, E-ISSN 1873-2917, Vol. 143, nr 1, s. 113-120Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Noninvasive genetic monitoring has the potential to estimate vital rates essential for conservation and management of many species. In a long-term genetic capture-mark-recapture study using scats we evaluated temporal variation in adult survival in a wolverine (Gulo gulo) population in southern Norway. In contrast to most previous studies of large mammals we found evidence for negative density dependence in adult survival in this large carnivore. Both sexes showed the same pattern of density dependence, with higher annual survival rates in adult females than males. In addition, we also found an additive mortality effect of harvesting in the population, resulting in the lowest adult survival rates at a combination of high population density and high harvest rate. The additive effects of density and harvest on adult survival of wolverines have relevance to the conservation and management of solitary carnivores with strong intrasexual territoriality, especially for species where combats among conspecifics can cause serious injury or even mortality.

  • 27.
    Burri, Reto
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nater, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Kawakami, Takeshi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina F.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ólason, Páll I.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för cell- och molekylärbiologi, Molekylär evolution.
    Smeds, Linnea
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Suh, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Dutoit, Ludovic
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Bures, Stanislav
    Palacky Univ, Dept Zool, Lab Ornithol, Olomouc 77146, Czech Republic..
    Garamszegi, Laszlo Z.
    CSIC, Dept Evolutionary Ecol, Estn Biol Donana, Seville 41092, Spain..
    Hogner, Silje
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway.;Univ Oslo, Nat Hist Museum, N-0318 Oslo, Norway..
    Moreno, Juan
    CSIC, Museo Nacl Ciencias Nat, E-28006 Madrid, Spain..
    Qvarnström, Anna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ruzic, Milan
    Bird Protect & Study Soc Serbia, Novi Sad 21000, Serbia..
    Saether, Stein-Are
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway.;Norwegian Inst Nat Res NINA, N-7034 Trondheim, Norway..
    Saetre, Glenn-Peter
    Univ Oslo, Ctr Ecol & Evolutionary Synth, Dept Biosci, N-0316 Oslo, Norway..
    Toeroek, Janos
    Eotvos Lorand Univ, Dept Systemat Zool & Ecol, Behav Ecol Grp, H-1117 Budapest, Hungary..
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers2015Ingår i: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 25, nr 11, s. 1656-1665Artikel i tidskrift (Refereegranskat)
    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.

  • 28.
    Corl, Ammon
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Sampling strategies for species trees: The effects on phylogenetic inference of the number of genes, number of individuals, and whether loci are mitochondrial, sex-linked, or autosomal2013Ingår i: Molecular Phylogenetics and Evolution, ISSN 1055-7903, E-ISSN 1095-9513, Vol. 67, nr 2, s. 358-366Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Systematists can now use multi-locus data to construct species trees that take into account the stochastic nature of gene tree divergence among populations. There is a need to evaluate the new methods for species tree reconstruction in order to determine what kinds of loci to use and the most effective sampling schemes in terms of numbers of genes and numbers of individuals per species. Here we study sampling strategies with an empirical data set for six shorebird species in which we sequenced I mitochondrial, 12 autosomal, and 12 Z-linked loci for >8 individuals/species. We found that sampling greater numbers of genes resulted in substantial improvements to the resolution of the species tree, but sampling greater numbers of individuals had minor effects. We found that Z-linked loci significantly outperformed autosomal loci at all levels of sampling, which likely resulted from the lower effective population size of the Z-linked loci. Therefore, sex-linked loci are likely to be a powerful tool for multi-locus phylogenetic studies. We found that adding a mitochondria] gene to a set of Z-linked or autosomal loci substantially improved the resolution of the tree. Overall, our results help evaluate how best to maximize phylogenetic resolution while minimizing the costs of sequencing and computation when performing species tree analyses.

  • 29.
    Corl, Ammon
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    The genomic signature of sexual selection in the genetic diversity of the sex chromosomes and autosomes2012Ingår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 66, nr 7, s. 2138-2149Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Genomic levels of variation can help reveal the selective and demographic forces that have affected a species during its history. The relative amount of genetic diversity observed on the sex chromosomes as compared to the autosomes is predicted to differ among monogamous and polygynous species. Many species show departures from the expectation for monogamy, but it can be difficult to conclude that this pattern results from variation in mating system because forces other than sexual selection can act upon sex chromosome genetic diversity. As a critical test of the role of mating system, we compared levels of genetic diversity on the Z chromosome and autosomes of phylogenetically independent pairs of shorebirds that differed in their mating systems. We found general support for sexual selection shaping sex chromosome diversity because most polygynous species showed relatively reduced genetic variation on their Z chromosomes as compared to monogamous species. Differences in levels of genetic diversity between the sex chromosomes and autosomes may therefore contribute to understanding the long-term history of sexual selection experienced by a species.

  • 30.
    Craig, Rory J.
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Univ Edinburgh, Sch Biol Sci, Inst Evolutionary Biol, Edinburgh, Midlothian, Scotland..
    Suh, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Wang, Mi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Natural selection beyond genes: Identification and analyses of evolutionarily conserved elements in the genome of the collared flycatcher (Ficedula albicollis)2018Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, nr 2, s. 476-492Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    It is becoming increasingly clear that a significant proportion of the functional sequence within eukaryotic genomes is noncoding. However, since the identification of conserved elements (CEs) has been restricted to a limited number of model organisms, the dynamics and evolutionary character of the genomic landscape of conserved, and hence likely functional, sequence is poorly understood in most species. Moreover, identification and analysis of the full suite of functional sequence are particularly important for the understanding of the genetic basis of trait loci identified in genome scans or quantitative trait locus mapping efforts. We report that similar to 6.6% of the collared flycatcher genome (74.0Mb) is spanned by similar to 1.28 million CEs, a higher proportion of the genome but a lower total amount of conserved sequence than has been reported in mammals. We identified >200,000 CEs specific to either the archosaur, avian, neoavian or passeridan lineages, constituting candidates for lineage-specific adaptations. Importantly, no less than similar to 71% of CE sites were nonexonic (52.6Mb), and conserved nonexonic sequence density was negatively correlated with functional exonic density at local genomic scales. Additionally, nucleotide diversity was strongly reduced at nonexonic conserved sites (0.00153) relative to intergenic nonconserved sites (0.00427). By integrating deep transcriptome sequencing and additional genome annotation, we identified novel protein-coding genes, long noncoding RNA genes and transposon-derived (exapted) CEs. The approach taken here based on the use of a progressive cactus whole-genome alignment to identify CEs should be readily applicable to nonmodel organisms in general and help to reveal the rich repertoire of putatively functional noncoding sequence as targets for selection.

  • 31.
    Dutoit, Ludovic
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Burri, Reto
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nater, Alexander
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina F.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Hans, Ellegren
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Genomic distribution and estimation of nucleotide diversity in natural populations: perspectives from the collared flycatcher (Ficedula albicollis) genome2017Ingår i: Molecular Ecology Resources, ISSN 1755-098X, E-ISSN 1755-0998, Vol. 17, nr 4, s. 586-597Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Properly estimating genetic diversity in populations of nonmodel species requires a basic understanding of how diversity is distributed across the genome and among individuals. To this end, we analysed whole-genome resequencing data from 20 collared flycatchers (genome size approximate to 1.1 Gb; 10.13 million single nucleotide polymorphisms detected). Genomewide nucleotide diversity was almost identical among individuals (mean = 0.00394, range = 0.00384-0.00401), but diversity levels varied extensively across the genome (95% confidence interval for 200-kb windows = 0.0013-0.0053). Diversity was related to selective constraint such that in comparison with intergenic DNA, diversity at fourfold degenerate sites was reduced to 85%, 3' UTRs to 82%, 5' UTRs to 70% and nondegenerate sites to 12%. There was a strong positive correlation between diversity and chromosome size, probably driven by a higher density of targets for selection on smaller chromosomes increasing the diversity-reducing effect of linked selection. Simulations exploring the ability of sequence data from a small number of genetic markers to capture the observed diversity clearly demonstrated that diversity estimation from finite sampling of such data is bound to be associated with large confidence intervals. Nevertheless, we show that precision in diversity estimation in large out-bred population benefits from increasing the number of loci rather than the number of individuals. Simulations mimicking RAD sequencing showed that this approach gives accurate estimates of genomewide diversity. Based on the patterns of observed diversity and the performed simulations, we provide broad recommendations for how genetic diversity should be estimated in natural populations.

  • 32.
    Dutoit, Ludovic
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Mugal, Carina
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Bolivar, Paulina
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Wang, Mi
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Nadachowska-Brzyska, Krystyna
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Smeds, Linnea
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Gustafsson, Lars
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Zooekologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Sex-biased gene expression, sexual antagonism and levels of genetic diversity in the collared flycatcher (Ficedula albicollis) genome2018Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 27, nr 18, s. 3572-3581Artikel i tidskrift (Övrigt vetenskapligt)
    Abstract [en]

    Theoretical work suggests that sexual conflict should promote the maintenance of genetic diversity by the opposing directions of selection on sexually antagonistic mutations in males and females. This prediction, so far not been empirically tested on a genome-wide scale, could potentially contribute towards genomic heterogeneity in levels of genetic diversity. We used large-scale population genomic and transcriptomic data from the collared flycatcher (Ficedula albicollis) to analyse how sex-biased gene expression – one outcome of sexual conflict – relates to genetic variability. Here, we demonstrate that the extent of sex-biased gene expression of both male-biased and female-biased genes is significantly correlated with levels of nucleotide diversity in gene sequences and that this correlation extends to the overall levels of genomic diversity. We find evidence for balancing selection in sex-biased genes, suggesting that sex-biased gene expression could be seen as a component counteracting the diversity-reducing effects of linked positive and purifying selection. The observation of significant genetic differentiation between males and females for male-biased genes indicates ongoing sexual conflict and sex-specific viability selection, potentially driven by sexual selection. Our results thus provide a new perspective on the long-standing question in evolutionary biology of how genomes can remain so genetically variable in face of strong natural and sexual selection.

  • 33.
    Dutoit, Ludovic
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Vijay, Nagarjun
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Univ Michigan, Dept Ecol & Evolutionary Biol, Lab Mol & Genom Evolut, Ann Arbor, MI USA..
    Mugal, Carina F.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Bossu, Christen M.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Stockholm Univ, Dept Zool, S-10691 Stockholm, Sweden.
    Burri, Reto
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Friedrich Schiller Univ, Inst Ecol, Dept Ecol, Dornburger Str 159 07743 Jena, Jena, Germany.
    Wolf, Jochen
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi. Ludwig Maximilians Univ Munchen, Fac Biol 2, Div Evolutionary Biol, Grosshaderner Str 2, D-82152 Martinsried, Germany..
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Covariation in levels of nucleotide diversity in homologous regions of the avian genome long after completion of lineage sorting2017Ingår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, nr 1849, artikel-id 20162756Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Closely related species may show similar levels of genetic diversity in homologous regions of the genome owing to shared ancestral variation still segregating in the extant species. However, after completion of lineage sorting, such covariation is not necessarily expected. On the other hand, if the processes that govern genetic diversity are conserved, diversity may potentially covary even among distantly related species. We mapped regions of conserved synteny between the genomes of two divergent bird speciescollared flycatcher and hooded crow-and identified more than 600 Mb of homologous regions (66% of the genome). From analyses of whole-genome resequencing data in large population samples of both species we found nucleotide diversity in 200 kb windows to be well correlated (Spearman's rho = 0.407). The correlation remained highly similar after excluding coding sequences. To explain this covariation, we suggest that a stable avian karyotype and a conserved landscape of recombination rate variation render the diversity-reducing effects of linked selection similar in divergent bird lineages. Principal component regression analysis of several potential explanatory variables driving heterogeneity in flycatcher diversity levels revealed the strongest effects from recombination rate variation and density of coding sequence targets for selection, consistent with linked selection. It is also possible that a stable karyotype is associated with a conserved genomic mutation environment contributing to covariation in diversity levels between lineages. Our observations imply that genetic diversity is to some extent predictable.

  • 34.
    Ekblom, Robert
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Brechlin, Birte
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Persson, Jens
    Swedish Univ Agr Sci, Dept Ecol, Grimso Wildlife Res Stn, Riddarhyttan, Sweden.
    Smeds, Linnea
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Johansson, Malin
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Magnusson, Jessica
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Flagstad, Oystein
    Norwegian Inst Nat Res, Trondheim, Norway.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Genome sequencing and conservation genomics in the Scandinavian wolverine population2018Ingår i: Conservation Biology, ISSN 0888-8892, E-ISSN 1523-1739, Vol. 32, nr 6, s. 1301-1312Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Genetic approaches have proved valuable to the study and conservation of endangered populations, especially for monitoring programs, and there is potential for further developments in this direction by extending analyses to the genomic level. We assembled the genome of the wolverine (Gulo gulo), a mustelid that in Scandinavia has recently recovered from a significant population decline, and obtained a 2.42 Gb draft sequence representing >85% of the genome and including >21,000 protein-coding genes. We then performed whole-genome resequencing of 10 Scandinavian wolverines for population genomic and demographic analyses. Genetic diversity was among the lowest detected in a red-listed population (mean genome-wide nucleotide diversity of 0.05%). Results of the demographic analyses indicated a long-term decline of the effective population size (N-e) from 10,000 well before the last glaciation to N-e appeared even lower. The genome-wide F-IS level was 0.089 (possibly signaling inbreeding), but this effect was not observed when analyzing a set of highly variable SNP markers, illustrating that such markers can give a biased picture of the overall character of genetic diversity. We found significant population structure, which has implications for population connectivity and conservation. We used an integrated microfluidic circuit chip technology to develop an SNP-array consisting of 96 highly informative markers that, together with a multiplex pre-amplification step, was successfully applied to low-quality DNA from scat samples. Our findings will inform management, conservation, and genetic monitoring of wolverines and serve as a genomic roadmap that can be applied to other endangered species. The approach used here can be generally utilized in other systems, but we acknowledge the trade-off between investing in genomic resources and direct conservation actions.

  • 35.
    Ekblom, Robert
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Johansson, Malin
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Magnusson, Jessica
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    DNA-analys av spillningsprover från järv: Genetisk metodutveckling, Slutrapport2016Rapport (Övrigt vetenskapligt)
  • 36.
    Ekblom, Robert
    et al.
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Smeds, Linnea
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Patterns of sequencing coverage bias revealed by ultra-deep sequencing of vertebrate mitochondria2014Ingår i: BMC Genomics, ISSN 1471-2164, E-ISSN 1471-2164, Vol. 15, s. 467-Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Background: Genome and transcriptome sequencing applications that rely on variation in sequence depth can be negatively affected if there are systematic biases in coverage. We have investigated patterns of local variation in sequencing coverage by utilising ultra-deep sequencing (>100,000X) of mtDNA obtained during sequencing of two vertebrate genomes, wolverine (Gulo gulo) and collared flycatcher (Ficedula albicollis). With such extreme depth, stochastic variation in coverage should be negligible, which allows us to provide a very detailed, fine-scale picture of sequence dependent coverage variation and sequencing error rates. Results: Sequencing coverage showed up to six-fold variation across the complete mtDNA and this variation was highly repeatable in sequencing of multiple individuals of the same species. Moreover, coverage in orthologous regions was correlated between the two species and was negatively correlated with GC content. We also found a negative correlation between the site-specific sequencing error rate and coverage, with certain sequence motifs "CCNGCC" being particularly prone to high rates of error and low coverage. Conclusions: Our results demonstrate that inherent sequence characteristics govern variation in coverage and suggest that some of this variation, like GC content, should be controlled for in, for example, RNA-Seq and detection of copy number variation.

  • 37.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    A selection model of molecular evolution incorporating the effective population size.2009Ingår i: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 63, nr 2, s. 301-305Artikel i tidskrift (Refereegranskat)
  • 38.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Characteristics, causes and evolutionary consequences of male-biased mutation2007Ingår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 274, nr 1606, s. 1-10Artikel, forskningsöversikt (Refereegranskat)
    Abstract [en]

    Mutation has traditionally been considered a random process, but this paradigm is challenged by recent evidence of divergence rate heterogeneity in different genomic regions. One facet of mutation rate variation is the propensity for genetic change to correlate with the number of germ cell divisions, reflecting the replication-dependent origin of many mutations. Haldane was the first to connect this association of replication and mutation to the difference in the number of cell divisions in oogenesis (low) and spermatogenesis (usually high), and the resulting sex difference in the rate of mutation. The concept of male-biased mutation has been thoroughly analysed in recent years using an evolutionary approach, in which sequence divergence of autosomes and/or sex chromosomes are compared to allow inference about the relative contribution of mothers and fathers in the accumulation of mutations. For instance, assuming that a neutral sequence is analysed, that rate heterogeneity owing to other factors is cancelled out by the investigation of many loci and that the effect of ancestral polymorphism is properly taken into account, the male-to-female mutation rate ratio, αm, can be solved from the observed difference in rate of X and Y chromosome divergence. The male mutation bias is positively correlated with the relative excess of cell divisions in the male compared to the female germ line, as evidenced by a generation time effect: in mammals, αm is estimated at approximately 4–6 in primates, approximately 3 in carnivores and approximately 2 in small rodents. Another life-history correlate is sexual selection: when there is intense sperm competition among males, increased sperm production will be associated with a larger number of mitotic cell divisions in spermatogenesis and hence an increase in αm. Male-biased mutation has implications for important aspects of evolutionary biology such as mate choice in relation to mutation load, sexual selection and the maintenance of genetic diversity despite strong directional selection, the tendency for a disproportionate large role of the X (Z) chromosome in post-zygotic isolation, and the evolution of sex.

  • 39.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Emergence of male-biased genes on the chicken Z-chromosome: Sex-chromosome contrasts between male and female heterogametic systems2011Ingår i: Genome Research, ISSN 1088-9051, E-ISSN 1549-5469, Vol. 21, nr 12, s. 2082-2086Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    There has been extensive traffic of male-biased genes out of the mammalian and Drosophila X-chromosomes, and there are also reports of an under-representation of male-biased genes on the X. This may reflect an adaptive process driven by natural selection where an autosomal location of male-biased genes is favored since male genes are only exposed to selection one-third of the time when X-linked. However, there are several alternative explanations to "out-of-the-X'' gene movement, including mutational bias and a means for X-linked genes to escape meiotic sex chromosome inactivation (MSCI) during spermatogenesis. As a critical test of the hypothesis that genomic relocation of sex-biased genes is an adaptive process, I examined the emergence, and loss, of genes on the chicken Z-chromosome, i.e., a female heterogametic system (males ZZ, females ZW). Here, the analogous prediction would be an emergence of male-biased genes onto, not a loss from, the Z-chromosome because Z is found more often in males than autosomes are. I found that genes expressed in testis but not in ovary are highly over-represented among genes that have emerged on the Z-chromosome during avian evolution. Moreover, genes with male-biased expression are similarly over-represented among new Z-chromosomal genes. Interestingly, genes with female-biased expression have more often moved from than to the Z-chromosome. These observations show that male and female heterogametic organisms display opposing directionalities in the emergence and loss of sex-biased genes on sex chromosomes. This is consistent with theoretical models on the evolution of sexually antagonistic genes in which new mutations are at least partly dominant.

  • 40.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    Evolution: Natural selection in the evolution of humans and chimps.2005Ingår i: Curren Biology, nr 22, s. R919-922Artikel i tidskrift (Refereegranskat)
  • 41.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Evolutionary stasis: the stable chromosomes of birds2010Ingår i: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 25, nr 5, s. 283-291Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Evolution at the molecular level is manifested in a variety of types of change in DNA sequences, including changes in the structure and organisation of chromosomes. However, in birds chromosomal evolution occurs at an unusually slow rate and recent whole-genome comparisons have shown that many chromosomes have remained more or less intact during avian evolution. Here I discuss progress in the development of genetic maps of natural bird populations, which has revealed that the evolutionary stasis of chromosomes often extends to conservation of gene order. The evolutionary stability of bird chromosomes, which might relate to a low frequency of transposable elements, will facilitate the transfer of genomic information from model to non-model organisms and might have a connection to the rarity of postzygotic incompatibilities observed in birds.

  • 42.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Genome sequencing and population genomics in non-model organisms2014Ingår i: Trends in Ecology & Evolution, ISSN 0169-5347, E-ISSN 1872-8383, Vol. 29, nr 1, s. 51-63Artikel, forskningsöversikt (Refereegranskat)
    Abstract [en]

    High-throughput sequencing technologies are revolutionizing the life sciences. The past 12 months have seen a burst of genome sequences from non-model organisms, in each case representing a fundamental source of data of significant importance to biological research. This has bearing on several aspects of evolutionary biology, and we are now beginning to see patterns emerging from these studies. These include significant heterogeneity in the rate of recombination that affects adaptive evolution and base composition, the role of population size in adaptive evolution, and the importance of expansion of gene families in lineage-specific adaptation. Moreover, resequencing of population samples (population genomics) has enabled the identification of the genetic basis of critical phenotypes and cast light on the landscape of genomic divergence during speciation.

  • 43.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolutionsbiologi. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Genomic evidence for a large-Z effect2009Ingår i: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 276, nr 1655, s. 361-366Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    The 'large-X effect' suggests that sex chromosomes play a disproportionate role in adaptive evolution. Theoretical work indicates that this effect may be most pronounced in genetic systems with female heterogamety under both good-genes and Fisher's runaway models of sexual selection (males ZZ, females ZW). Here, I use a comparative genomic approach (alignments of several thousands of chicken-zebra finch-human-mouse-opossum orthologues) to show that avian Z-linked genes are highly overrepresented among those bird-mammalian orthologues that show evidence of accelerated rate of functional evolution in birds relative to mammals; the data suggest a twofold excess of such genes on the Z chromosome. A reciprocal analysis of genes accelerated in mammals found no evidence for an excess of X-linkage. This would be compatible with theoretical expectations for differential selection on sex-linked genes under male and female heterogamety, although the power in this case was not sufficient to statistically show that 'large-Z' was more pronounced than 'large-X'. Accelerated Z-linked genes include a variety of functional categories and are characterized by higher non-synonymous to synonymous substitution rate ratios than both accelerated autosomal and non-accelerated genes. This points at a genomic 'large-Z effect', which is widespread and of general significance for adaptive divergence in birds.

  • 44.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Hvad nytt och nyttigt: Tillkomsten av Sveriges första lärda sällskap: Kungl. Vetenskaps-Societeten i Uppsala2019Bok (Övrigt vetenskapligt)
    Abstract [sv]

    Kungl. Vetenskaps-Societeten i Uppsala är Sveriges äldsta lärda sällskap, vår första vetenskapsakademi. Den har sitt ursprung i det Collegium Curiosorum som den framsynte bibliotekarien Erik Benzelius d.y. samlade 1710. Det var i en tid då teologin och humaniora ännu dominerade i lärdomsstaden. Men den vetenskapliga revolutionen drog fram genom Europa och på kontinenten hade vetenskapare börjat organisera sig i akademier. Inspiration hämtades därifrån.

    Sällskapet korresponderar med Christopher Polhem kring den nya naturvetenskapen. De skickar ut den unge Emanuel Swedenborg för att bevaka den internationella forskningsfronten. Verksamheten utvecklas och man börjar ger ut landets första vetenskapstidskrift, Acta Literaria Sveciæ. Genom förarbete av Arvid Horn beslutar så Fredrik I 1728 om inrättandet av Kungl. Vetenskaps--Societeten. Under nära 20 år är det Anders Celsius som leder organisationen.

    Societetens inledande stadgar utgjorde ett patriotiskt forskningsprogram. Att lyfta fram landets naturtillgångar och unika resurser var viktigt. Ett tecken på detta är att man använder nästan hela sin kassa för att finansiera Linnés lappländska resa 1732. 

    Röster höjs dock för att frångå latinet till förmån för publicering på svenska, för att nå ut med nyttiga rön i samhället snarare än att söka internationell spridning. Dessutom föreslås att verksamheten ska flytta till Stockholm. I Hvad nytt och nyttigt beskriver Hans Ellegren händelser under 1700-talets första del, då vetenskapen började bedrivas på ett sätt som känns igen än idag. I arbetet kommer författaren i kontakt med kollegor från en annan tid, och lär känna deras personligheter och egenheter. 

  • 45.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Is genetic diversity really higher in large populations?2009Ingår i: Journal of Biology, ISSN 1478-5854, E-ISSN 1475-4924, Vol. 8, nr 4, s. 41-Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Analyses of mitochondrial DNA (mtDNA) have challenged the concept that genetic diversity within populations is governed by effective population size and mutation rate. A recent study in BMC Evolutionary Biology shows that variation in the rate of mutation rather than in population size is the main explanation for variations in mtDNA diversity observed among bird species.

  • 46.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Platypus genome suggests a recent origin for the human X.2008Ingår i: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 18, nr 13, s. R557-R559Artikel i tidskrift (Refereegranskat)
  • 47.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Processer för ökad forskningskvalitet: Rapport från uppföljning av KoF-utvärderingarna och verksamhetens syn på forskningsutvärderingar2015Rapport (Övrig (populärvetenskap, debatt, mm))
  • 48.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för evolution, genomik och systematik, Evolutionsbiologi.
    Sequencing goes 454 and takes large-scale genomics into the wild2008Ingår i: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 17, nr 7, s. 1629-1631Artikel i tidskrift (Refereegranskat)
    Abstract [en]

    Sometimes, science takes a big leap forward. This is often due to new technology that allows the study of questions previously difficult or even impossible to address. An example of this is provided in this issue (Vera et al. 2008) by the first large-scale attempt toward genome sequencing of an ecologically important model, based on the new '454-sequencing technology'. Using this new technology, the protein-coding sequences of the Glanville fritillary butterfly genome have now been largely characterized.

  • 49.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Biologiska sektionen, Institutionen för ekologi och genetik, Evolutionsbiologi.
    Sex-chromosome evolution: recent progress and the influence of male and female heterogamety2011Ingår i: Nature reviews genetics, ISSN 1471-0056, E-ISSN 1471-0064, Vol. 12, nr 3, s. 157-166Artikel, forskningsöversikt (Refereegranskat)
    Abstract [en]

    It is now clear that sex chromosomes differ from autosomes in many aspects of genome biology, such as organization, gene content and gene expression. Moreover, sex linkage has numerous evolutionary genetic implications. Here, I provide a coherent overview of sex-chromosome evolution and function based on recent data. Heteromorphic sex chromosomes are almost as widespread across the animal and plant kingdoms as sexual reproduction itself and an accumulating body of genetic data reveals interesting similarities, as well as dissimilarities, between organisms with XY or ZW sex-determination systems. Therefore, I discuss how patterns and processes associated with sex linkage in male-and female-heterogametic systems offer a useful contrast in the study of sex-chromosome evolution.

  • 50.
    Ellegren, Hans
    Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik. Uppsala universitet, Teknisk-naturvetenskapliga vetenskapsområdet, Teknisk-naturvetenskapliga fakulteten, Institutionen för evolution, genomik och systematik, Evolutionsbiologi. Evolutionsbiologi.
    The avian genome uncovered.2005Ingår i: Trends in Ecology and Evolution, nr 20, s. 180-186Artikel i tidskrift (Refereegranskat)
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