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The genomic signature of dog domestication reveals adaptation to a starch-rich diet

Abstract

The domestication of dogs was an important episode in the development of human civilization. The precise timing and location of this event is debated1,2,3,4,5 and little is known about the genetic changes that accompanied the transformation of ancient wolves into domestic dogs. Here we conduct whole-genome resequencing of dogs and wolves to identify 3.8 million genetic variants used to identify 36 genomic regions that probably represent targets for selection during dog domestication. Nineteen of these regions contain genes important in brain function, eight of which belong to nervous system development pathways and potentially underlie behavioural changes central to dog domestication6. Ten genes with key roles in starch digestion and fat metabolism also show signals of selection. We identify candidate mutations in key genes and provide functional support for an increased starch digestion in dogs relative to wolves. Our results indicate that novel adaptations allowing the early ancestors of modern dogs to thrive on a diet rich in starch, relative to the carnivorous diet of wolves, constituted a crucial step in the early domestication of dogs.

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Figure 1: Selection analyses identified 36 candidate domestication regions.
Figure 2: Selection for increased amylase activity.
Figure 3: Selection is associated with increased maltase activity.

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Accession codes

Primary accessions

Sequence Read Archive

Data deposits

Sequence reads are available under the accession number SRA061854 (NCBI Sequence Read Archive).

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Acknowledgements

We thank Järvzoo, Nordens ark and the Canine Biobank at Uppsala University and the Swedish University of Agricultural Sciences for providing samples, Uppsala Genomics Platform at SciLifeLab Uppsala for generating the resequencing data, the UPPNEX platform for assisting with computational infrastructure for data analysis and the Broad Institute Genomics Platform for validation genotyping. The project was funded by the SSF, the Swedish Research Council, the Swedish Research Council Formas, Uppsala University and a EURYI to K.L.-T. funded by the ESF supporting also E.A.; K.M. was funded by the Higher Education Commission, Pakistan.

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Authors and Affiliations

Authors

Contributions

K.L.-T. and Å.H. designed the study. K.L.-T. and E.A. oversaw the study. M.-L.A. coordinated and performed the majority of the sample collecting and O.L. and J.M.A. provided samples of critical importance. E.A. performed the SNP detection and selection analyses; A.R. identified candidate causative mutations and analysed haplotypes in CDRs; K.M. detected CNVs bioinformatically; M.T.W. performed phylogenetic analysis and analysed the Canine HD-array data; A.R. performed the maltase activity assay; M.-L.A. validated CNVs and quantified mRNA expression of candidate genes; M.P. performed validation SNP genotyping; E.A., A.R., M.-L.A. and K.L-T. interpreted the data; E.A. and K.L.-T. wrote the paper with input from the other authors.

Corresponding authors

Correspondence to Erik Axelsson or Kerstin Lindblad-Toh.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Discussions sections 1-9, Supplementary references, Supplementary Figures 1-24 and Supplementary Tables 1-25. (PDF 6581 kb)

Supplementary Data 1

This zipped file lists the position of short indels in the canine genome. (ZIP 3569 kb)

Supplementary Data 2

This zipped file lists the position of CNVs in the canine genome. (ZIP 257 kb)

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Axelsson, E., Ratnakumar, A., Arendt, ML. et al. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495, 360–364 (2013). https://doi.org/10.1038/nature11837

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