Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours

Anna V. Kukekova; Jennifer L. Johnson; Xueyan Xiang; Shaohong Feng; Shiping Liu; Halie M. Rando; Anastasiya V. Kharlamova; Yury Herbeck; Natalya A. Serdyukova; Zijun Xiong; Violetta Beklemischeva; Klaus Peter Koepfli; Rimma G. Gulevich; Anastasiya V. Vladimirova; Jessica P. Hekman; Polina L. Perelman; Aleksander S. Graphodatsky; Xu Wang; Andrew G. Clark; Gregory M. Acland; Lyudmila N. Trut; Guojie Zhang; Stephen James O'Brien

doi:10.1038/s41559-018-0611-6

Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours

Anna V. Kukekova
, Jennifer L. Johnson
, Xueyan Xiang
, Shaohong Feng
, Shiping Liu
, Halie M. Rando
, Anastasiya V. Kharlamova
, Yury Herbeck
, Natalya A. Serdyukova
, Zijun Xiong
, Violetta Beklemischeva
, Klaus Peter Koepfli
, Rimma G. Gulevich
, Anastasiya V. Vladimirova
, Jessica P. Hekman
, Polina L. Perelman
, Aleksander S. Graphodatsky
, Xu Wang
, Andrew G. Clark
, Gregory M. Acland

Lyudmila N. Trut, Guojie Zhang, Stephen James O'Brien

Department of Biological Sciences

Research output: Contribution to journal › Article › peer-review

115 Scopus citations

Abstract

Strains of red fox (Vulpes vulpes) with markedly different behavioural phenotypes have been developed in the famous long-term selective breeding programme known as the Russian farm-fox experiment. Here we sequenced and assembled the red fox genome and re-sequenced a subset of foxes from the tame, aggressive and conventional farm-bred populations to identify genomic regions associated with the response to selection for behaviour. Analysis of the re-sequenced genomes identified 103 regions with either significantly decreased heterozygosity in one of the three populations or increased divergence between the populations. A strong positional candidate gene for tame behaviour was highlighted: SorCS1, which encodes the main trafficking protein for AMPA glutamate receptors and neurexins and suggests a role for synaptic plasticity in fox domestication. Other regions identified as likely to have been under selection in foxes include genes implicated in human neurological disorders, mouse behaviour and dog domestication. The fox represents a powerful model for the genetic analysis of affiliative and aggressive behaviours that can benefit genetic studies of behaviour in dogs and other mammals, including humans.

Original language	American English
Pages (from-to)	1479-1491
Number of pages	13
Journal	Nature Ecology & Evolution
Volume	2
Issue number	9
DOIs	https://doi.org/10.1038/s41559-018-0611-6
State	Published - Sep 1 2018

Bibliographical note

Publisher Copyright:
© 2018, The Author(s).

Funding

We are grateful to I.V. Pivovarova, T.I. Semenova and all the animal keepers at the ICG experimental farm for research assistance. The project was supported by National Institutes of Health grant GM120782, USDA Federal Hatch Project 538922, the Russian Science Foundation grants 16-14-10009 and 16-14-10216 (animal behaviour analysis, sample collection and analysis), the Institute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences grant 0324-2018-0016 (animal maintenance), grants from Campus Research Board and Office of International Programs of the University of Illinois at Urbana-Champaign. The project was also supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant XDB13000000), Lundbeck fellowship for G.Z. (R190-2014-2827) and the Carlsberg Foundation grant CF16-0663.

Funders	Funder number
Office of International Programs of the University of Illinois at Urbana-Champaign
National Institutes of Health
National Institute of General Medical Sciences	R01GM120782
U.S. Department of Agriculture	538922
Campus Research Board
Chinese Academy of Sciences	XDB13000000
Carlsbergfondet	CF16-0663
Siberian Branch, Russian Academy of Sciences	0324-2018-0016
Russian Science Foundation	16-14-10009, 16-14-10216
H. Lundbeck A/S	R190-2014-2827

ASJC Scopus Subject Areas

Ecology, Evolution, Behavior and Systematics
Ecology

Keywords

Behavior, Animal
Foxes/physiology
Animals
Aggression
Female
Male
Genome

Disciplines

Genetics and Genomics
Life Sciences

Access to Document

10.1038/s41559-018-0611-6

S41559 018 0611 6Final published version, 631 KBLicense: Unspecified

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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., Beklemischeva, V., Koepfli, K. P., Gulevich, R. G., Vladimirova, A. V., Hekman, J. P., Perelman, P. L., Graphodatsky, A. S., Wang, X., Clark, A. G., ... O'Brien, S. J. (2018). Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours. Nature Ecology & Evolution, 2(9), 1479-1491. https://doi.org/10.1038/s41559-018-0611-6

Kukekova, AV, Johnson, JL, Xiang, X, Feng, S, Liu, S, Rando, HM, Kharlamova, AV, Herbeck, Y, Serdyukova, NA, Xiong, Z, Beklemischeva, V, Koepfli, KP, Gulevich, RG, Vladimirova, AV, Hekman, JP, Perelman, PL, Graphodatsky, AS, Wang, X, Clark, AG, Acland, GM, Trut, LN, Zhang, G & O'Brien, SJ 2018, 'Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours', Nature Ecology & Evolution, vol. 2, no. 9, pp. 1479-1491. https://doi.org/10.1038/s41559-018-0611-6

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abstract = " Strains of red fox (Vulpes vulpes) with markedly different behavioural phenotypes have been developed in the famous long-term selective breeding programme known as the Russian farm-fox experiment. Here we sequenced and assembled the red fox genome and re-sequenced a subset of foxes from the tame, aggressive and conventional farm-bred populations to identify genomic regions associated with the response to selection for behaviour. Analysis of the re-sequenced genomes identified 103 regions with either significantly decreased heterozygosity in one of the three populations or increased divergence between the populations. A strong positional candidate gene for tame behaviour was highlighted: SorCS1, which encodes the main trafficking protein for AMPA glutamate receptors and neurexins and suggests a role for synaptic plasticity in fox domestication. Other regions identified as likely to have been under selection in foxes include genes implicated in human neurological disorders, mouse behaviour and dog domestication. The fox represents a powerful model for the genetic analysis of affiliative and aggressive behaviours that can benefit genetic studies of behaviour in dogs and other mammals, including humans.",

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AU - Rando, Halie M.

AU - Kharlamova, Anastasiya V.

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AU - Xiong, Zijun

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AU - Wang, Xu

AU - Clark, Andrew G.

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AU - Zhang, Guojie

AU - O'Brien, Stephen James

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Red fox genome assembly identifies genomic regions associated with tame and aggressive behaviours

Abstract

Bibliographical note

Funding

ASJC Scopus Subject Areas

Keywords

Disciplines

Access to Document

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