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Edited by Montgomery Slatkin, University of California, Berkeley, CA, and approved November 16, 2015 (received for review June 25, 2015)
Significance
Dogs have an integral role in human society, and recent evidence suggests they have a unique bond that elicits a beneficial hormonal response in both dogs and human handlers. Here, we show this relationship has a dark side. Small population size during domestication and strong artificial selection for breed-defining traits has unintentionally increased the numbers of deleterious genetic variants. Our findings question the overly typological practice of breeding individuals that best fit breed standards, a Victorian legacy. This practice does not allow selection to remove potentially deleterious variation associated with genes responsible for breed-specific traits.
Abstract
Population bottlenecks, inbreeding, and artificial selection can all, in principle, influence levels of deleterious genetic variation. However, the relative importance of each of these effects on genome-wide patterns of deleterious variation remains controversial. Domestic and wild canids offer a powerful system to address the role of these factors in influencing deleterious variation because their history is dominated by known bottlenecks and intense artificial selection. Here, we assess genome-wide patterns of deleterious variation in 90 whole-genome sequences from breed dogs, village dogs, and gray wolves. We find that the ratio of amino acid changing heterozygosity to silent heterozygosity is higher in dogs than in wolves and, on average, dogs have 2–3% higher genetic load than gray wolves. Multiple lines of evidence indicate this pattern is driven by less efficient natural selection due to bottlenecks associated with domestication and breed formation, rather than recent inbreeding. Further, we find regions of the genome implicated in selective sweeps are enriched for amino acid changing variants and Mendelian disease genes. To our knowledge, these results provide the first quantitative estimates of the increased burden of deleterious variants directly associated with domestication and have important implications for selective breeding programs and the conservation of rare and endangered species. Specifically, they highlight the costs associated with selective breeding and question the practice favoring the breeding of individuals that best fit breed standards. Our results also suggest that maintaining a large population size, rather than just avoiding inbreeding, is a critical factor for preventing the accumulation of deleterious variants.
Footnotes
↵1C.D.M. and D.O.-D.V. contributed equally to this work.
- ↵2To whom correspondence should be addressed. Email: klohmueller{at}ucla.edu.
Author contributions: C.D.M., D.O.-D.V., D.P.O., J.F.T., O.R., C.V., T.M.-B., R.D.S., R.K.W., and K.E.L. designed research; C.D.M., D.O.-D.V., D.P.O., J.F.T., O.R., C.V., T.M.-B., R.D.S., and K.E.L. performed research; D.P.O., J.F.T., O.R., C.V., T.M.-B., R.D.S., R.K.W., and K.E.L. contributed new reagents/analytic tools; C.D.M., D.O.-D.V., and K.E.L. analyzed data; and C.D.M., D.O.-D.V., R.K.W., and K.E.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Database deposition: NCBI Sequence Read Archive accessions for previously unpublished genomes are in Dataset S1. The data reported in this paper have been deposited in the Dryad Digital Repository, datadryad.org (doi:10.5061/dryad.012s5).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1512501113/-/DCSupplemental.
http://www.pnas.org/preview_site/misc/userlicense.xhtml
Deleterious genetic variants in dogs and wolves
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