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An extensive candidate gene approach to speciation: diversity, divergence and linkage disequilibrium in candidate pigmentation genes across the European crow hybrid zone
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
2013 (English)In: Heredity, ISSN 0018-067X, E-ISSN 1365-2540, Vol. 111, no 6, 467-473 p.Article in journal (Refereed) Published
Abstract [en]

Colouration patterns have an important role in adaptation and speciation. The European crow system, in which all-black carrion crows and grey-coated hooded crows meet in a narrow hybrid zone, is a prominent example. The marked phenotypic difference is maintained by assortative mating in the absence of neutral genetic divergence, suggesting the presence of few pigmentation genes of major effect. We made use of the rich phenotypic and genetic resources in mammals and identified a comprehensive panel of 95 candidate pigmentation genes for birds. Based on functional annotation, we chose a subset of the most promising 37 candidates, for which we developed a marker system that demonstrably works across the avian phylogeny. In total, we sequenced 107 amplicons (~3 loci per gene, totalling 60 kb) in population samples of crows (n=23 for each taxon). Tajima’s D, Fu’s FS, DHEW and HKA (Hudson–Kreitman–Aguade) statistics revealed several amplicons that deviated from neutrality; however, none of these showed significantly elevated differentiation between the two taxa. Hence, colour divergence in this system may be mediated by uncharacterized pigmentation genes or regulatory regions outside genes. Alternatively, the observed high population recombination rate (4Ner~0.03), with overall linkage disequilibrium dropping rapidly within the order of few 100 bp, may compromise the power to detect causal loci with nearby markers. Our results add to the debate as to the utility of candidate gene approaches in relation to genomic features and the genetic architecture of the phenotypic trait in question.

Place, publisher, year, edition, pages
2013. Vol. 111, no 6, 467-473 p.
Keyword [en]
speciation, population genetics, bird colouration, pigmentation genes, recombination rate, linkage disequilibrium
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-209238DOI: 10.1038/hdy.2013.68ISI: 000327178100003OAI: oai:DiVA.org:uu-209238DiVA: diva2:656420
Available from: 2013-10-15 Created: 2013-10-15 Last updated: 2017-12-06Bibliographically approved
In thesis
1. The Genetics of Speciation and Colouration in Carrion and Hooded Crows
Open this publication in new window or tab >>The Genetics of Speciation and Colouration in Carrion and Hooded Crows
2013 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

A fundamental goal in biological research is to gain an understanding of the evolutionary processes and genetic elements that drive speciation. Genes responsible for reproductive isolation in young divergent lineages are particularly poorly known. In this thesis, the speciation genetics of carrion (Corvus (corone) corone) and hooded (C. (corone) cornix) crows were studied. These taxa differ strikingly in colouration and meet in a narrow hybrid zone in Europe, yet appear to be very similar genetically. A major component of reproductive isolation is social selection on colour differences.

First, we investigated the genetic basis of plumage divergence between carrion and hooded crows using a candidate gene approach. Nucleotide divergence was confirmed to be low, while there was no evidence for any of the sequenced genes to be associated with colour differences.

Second, we performed a simulation study to assess the performance of RNA-seq, a relatively novel approach that we later employed ourselves. We asked how variation in transcriptome complexity and bioinformatic workflow affected the accuracy of gene expression profiling. We generally found reassuring robustness and made a number of specific recommendations.

Third, we compared the corticosterone stress response of carrion and hooded crows. In accordance with the hypothesis that the degree of melanization and physiological traits are correlated due to pleiotropy, we found a higher stress response in hooded crows, and detected possibly associated gene expression in pituitary.

Fourth, we investigated genomic divergence by assembling a hooded crow reference genome followed by whole-genome resequencing of four European population samples. Northern European carrion crows were more similar to hooded crows than to Spanish carrion crows, pointing towards rampant introgression far beyond the hybrid zone. Nevertheless, several narrow genomic regions harboured high between-taxon divergence and were potentially associated with phenotypic traits.

Fifth, we compared whole-transcriptome gene expression profiles between crows, focusing on skin with developing feathers. We used a design that allowed to differentiate between taxon-specific, colour-specific and body patterning effects. Widespread underexpression of genes in the melanogenesis pathway was associated with grey colour, and we detected several genes that may contribute to colour divergence in this system.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2013. 48 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1088
Keyword
evolutionary genetics, genomics, birds, next-generation sequencing, pigmentation, pigmentation genetics, eumelanin, social selection, gene expression, population genomics
National Category
Evolutionary Biology
Research subject
Biology with specialization in Evolutionary Genetics
Identifiers
urn:nbn:se:uu:diva-209243 (URN)978-91-554-8777-5 (ISBN)
Public defence
2013-11-29, Lindahlssalen, Evolutionary Biology Centre, Norbyvägen 18D, Uppsala, 13:00 (English)
Opponent
Supervisors
Available from: 2013-11-08 Created: 2013-10-15 Last updated: 2014-01-23

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Poelstra, Jelmer W.Ellegren, HansWolf, Jochen

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