Demographically-based evaluation of genomic regions under selection in domestic dogs
Open accessAbstract
Controlling for background demographic effects is important for accurately identifying loci that have recently undergone positive selection. To date, the effects of demography have not yet been explicitly considered when identifying loci under selection during dog domestication. To investigate positive selection on the dog lineage early in the domestication, we examined patterns of polymorphism in six canid genomes that were previously used to infer a demographic model of dog domestication. Using an inferred demographic model, we computed false discovery rates (FDR) and identified 349 outlier regions consistent with positive selection at a low FDR. The signals in the top 100 regions were frequently centered on candidate genes related to brain function and behavior, including LHFPL3, CADM2, GRIK3, SH3GL2, MBP, PDE7B, NTAN1, and GLRA1. These regions contained significant enrichments in behavioral ontology categories. The 3rd top hit, CCRN4L, plays a major role in lipid metabolism, that is supported by additional metabolism related candidates revealed in our scan, including SCP2D1 and PDXC1. Comparing our method to an empirical outlier approach that does not directly account for demography, we found only modest overlaps between the two methods, with 60% of empirical outliers having no overlap with our demography-based outlier detection approach. Demography-aware approaches have lower-rates of false discovery. Our top candidates for selection, in addition to expanding the set of neurobehavioral candidate genes, include genes related to lipid metabolism, suggesting a dietary target of selection that was important during the period when proto-dogs hunted and fed alongside hunter-gatherers.
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These results are in line with claims in other studies on domestication, where categories like 'neurological process' frequently stand out strongly in gene ontology category enrichment analyses.
“These results are in line with claims in other studies on domestication [49, 123–125], where categories like ‘neurological process’ frequently stand out strongly in gene ontology category enrichment analyses.”
From Self-domestication in Homo sapiens: Insights from comparative genomics (2017) · cites this paper as [49]
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Minelli, A., Scassellati, C., Bonvicini, C., Pérez, J., & Gennarelli, M. (2009) · Neuropsychobiology · doi:10.1159/000202827 · Cited by 20 · see citing works
Balogh, S. A., McDowell, C. S., Kwon, Y. T., & Denenberg, V. H. (2001) · Brain Research · doi:10.1016/s0006-8993(00)03268-6 · Cited by 18 · see citing works
Modulation of social behavior by the agouti pigmentation gene
Carola, V., Perlas, E., Zonfrillo, F., et al. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00259 · Cited by 11 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [87]Slatkin M, Wiehe T (1998) Genetic hitch-hiking in a subdivided population. Genetical Res 71: 155– 160. 9717437
Cited by
Sorted by citations
Pendleton, A. L., Shen, F., Taravella, A. M., Emery, S., Veeramah, K. R., Boyko, A. R., & Kidd, J. M. (2018) · BMC Biology · doi:10.1186/s12915-018-0535-2 · Cited by 156 · see citing works
Self-citationSelf-domestication in Homo sapiens: Insights from comparative genomics
Theofanopoulou, C., Gastaldon, S., O’Rourke, T., Samuels, B. D., Messner, A., Martins, P. T., Delogu, F., Alamri, S., & Boeckx, C. (2017) · PLOS ONE · doi:10.1371/journal.pone.0185306 · Cited by 174 · see citing works
Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours
Kukekova, A. V., Johnson, J. L., Xiang, X., Feng, S., Liu, S., Rando, H. M., Kharlamova, A. V., Herbeck, Y., Serdyukova, N. A., Xiong, Z., et al. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0611-6 · Cited by 145 · see citing works
Highly heritable and functionally relevant breed differences in dog behaviour
MacLean, E. L., Snyder-Mackler, N., vonHoldt, B. M., & Serpell, J. A. (2019) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2019.0716 · Cited by 144 · see citing works
Glutamate receptors in domestication and modern human evolution
O’Rourke, T., & Boeckx, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.10.004 · Cited by 50 · see citing works
Evolutionary History, Selective Sweeps, and Deleterious Variation in the Dog
Freedman, A. H., Lohmueller, K. E., & Wayne, R. K. (2016) · Annual Review of Ecology, Evolution, and Systematics · doi:10.1146/annurev-ecolsys-121415-032155 · Cited by 50 · see citing works
Self-citation
- Authors
- Freedman, A. H., Schweizer, R. M., Ortega-Del Vecchyo, D., Han, E., Davis, B. W., Gronau, I., Silva, P. M., Galaverni, M., Fan, Z., Marx, P., Lorente-Galdos, B., Ramirez, O., Hormozdiari, F., Alkan, C., Vilà, C., Squire, K., Geffen, E., Kusak, J., Boyko, A. R., Parker, H. G., Lee, C., Tadigotla, V., Siepel, A., Bustamante, C. D., Harkins, T. T., Nelson, S. F., Marques-Bonet, T., Ostrander, E. A., Wayne, R. K., & Novembre, J.
- Affiliations
- University of California, Los Angeles (US)
- National Institutes of Health (US)
- Cornell University (US)
- Universidade do Porto (PT)
- Istituto Superiore per la Protezione e la Ricerca Ambientale (IT)
- Sichuan University (CN)
- Bilkent University (TR)
- Consejo Superior de Investigaciones Científicas (ES)
- Tel Aviv University (IL)
- University of Zagreb (HR)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- Cold Spring Harbor Laboratory (US)
- Stanford Medicine (US)
- Corresponding author
- Freedman, Adam H.
- ORCID
- Freedman, Adam H.
- Schweizer, Rena M.
- Davis, Brian W.
- Gronau, Ilan
- Silva, Pedro M.
- Galaverni, Marco
- Fan, Zhenxin
- Hormozdiari, Farhad
- Alkan, Can
- Vilà, Carles
- Geffen, Eli
- Kusak, Josip
- Boyko, Adam R.
- Parker, Heidi G.
- Lee, Clarence
- Siepel, Adam
- Bustamante, Carlos D.
- Harkins, Timothy T.
- Nelson, Stanley F.
- Ostrander, Elaine A.
- Wayne, Robert K.
- Novembre, John
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-03-04
- Volume
- 12
- Issue
- 3
- Pages
- e1005851
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC4778760
- OpenAlex
- W2292190728
- Cited by
- 104
- References
- 92
- Citations by year
- 2026: 3 · 2025: 8 · 2024: 3 · 2023: 7 · 2022: 7 · 2021: 14 · 2020: 15 · 2019: 15 · 2018: 14 · 2017: 13 · 2016: 5
- FWCI
- 12.62
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- public-domain
- creativecommons.org/publicdomain/zero/1.0/ (vor)
- Locations
- PLoS Genetics (publishedVersion, public-domain)
- Europe PMC (PubMed Central) (publishedVersion, public-domain)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- RECERCAT (Consorci de Serveis Universitaris de Catalunya) (publishedVersion, other-oa)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (acceptedVersion)
- Bilkent University Institutional Repository (Bilkent University) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, public-domain)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, public-domain)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Repositori digital de la UPF (Universitat Pompeu Fabra) (submittedVersion, public-domain)
- Funders
- Harvard University
- Tel Aviv University
- University of California, Los Angeles
- Institute for Digital Research and Education, University of California, Los Angeles
- FAS Division of Science, Harvard University
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
- Keywords
- dog domestication, positive selection, demographic effects, false discovery rate, candidate genes, lipid metabolism, dietary selection, hunter-gatherers
- MeSH terms
- Animals, Demography, Dogs, Genetics, Population, Selection, Genetic, Genome, Polymorphism, Single Nucleotide, Genomics, Lipid Metabolism
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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