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Genomic analysis of dingoes identifies genomic regions under reversible selection during domestication and feralization

Shao-jie Zhang, Guo-Dong Wang, Pengcheng Ma, Liang-liang Zhang, Ting-Ting Yin, Yan-hu Liu, Newton O. Otecko, Meng Wang, Ya-ping Ma, Lu Wang, Bingyu Mao, Peter Savolainen, Ya-ping Zhang
doi: https://doi.org/10.1101/472084
Shao-jie Zhang
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
bLaboratory for Conservation and Utilization of Bio-Resources & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming 650091, China.
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Guo-Dong Wang
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
cCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.
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Pengcheng Ma
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
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Liang-liang Zhang
dKTH Royal Institute of Technology, School of Engineering Sciences in Chemistry, Biotechnology and Health, Department of Gene Technology, Science for Life Laboratory, SE-171 65, Solna, Sweden.
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Ting-Ting Yin
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
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Yan-hu Liu
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
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Newton O. Otecko
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
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Meng Wang
bLaboratory for Conservation and Utilization of Bio-Resources & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming 650091, China.
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Ya-ping Ma
bLaboratory for Conservation and Utilization of Bio-Resources & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming 650091, China.
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Lu Wang
bLaboratory for Conservation and Utilization of Bio-Resources & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming 650091, China.
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Bingyu Mao
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
cCenter for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.
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  • For correspondence: mao@mail.kiz.ac.cn savo@biotech.kth.se zhangyp@mail.kiz.ac.cn
Peter Savolainen
dKTH Royal Institute of Technology, School of Engineering Sciences in Chemistry, Biotechnology and Health, Department of Gene Technology, Science for Life Laboratory, SE-171 65, Solna, Sweden.
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  • For correspondence: mao@mail.kiz.ac.cn savo@biotech.kth.se zhangyp@mail.kiz.ac.cn
Ya-ping Zhang
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
bLaboratory for Conservation and Utilization of Bio-Resources & Key Laboratory for Microbial Resources of the Ministry of Education, Yunnan University, Kunming 650091, China.
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  • For correspondence: mao@mail.kiz.ac.cn savo@biotech.kth.se zhangyp@mail.kiz.ac.cn
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Abstract

Dingoes (Canis dingo) are wild canids living in Australia. They have lived isolated from both the wild and the domestic ancestor and are a unique model for studying feralization, the process in which a domestic species escapes human control, adapts to the wild, and diverges from the domestic ancestor into a genetically distinct population. Here, we sequenced the genomes of 10 dingoes and 2 New Guinea Singing Dogs, to study the origins and feralization process of the dingo. Phylogenetic and demographic analyses show that dingoes originate from domestic dogs in southern East Asia, which migrated via Island Southeast Asia to reach Australia 4300-5000 years ago, and subsequently diverged into a genetically distinct population. Selection analysis identified 99 positively selected genes enriched in starch and fat metabolism pathways, indicating a diet change during feralization of dingoes. Interestingly, we found that 14 genes have shifted allele frequencies compared to dogs but not compared to wolves. This suggests that the selection affecting these genes during domestication of the wolf was reversed in the feralization process. One of these genes, ARHGEF7, may promote the formation of neural spine and synapses in hippocampal neurons. Functional assays showed that an A to G mutation in ARHGEF7, located in a transcription factor-binding site, decreases the endogenous expression. This suggests that ARHGEF7 may have been under selection for behavioral adaptations related to the transitions in environment both from wild to domestic and from domestic back to wild. Our results indicate that adaptation to domestication and feralization primarily affected different genomic regions, but that some genes, related to neurodevelopment, metabolism and reproduction, may have been reversibly affected in the two processes.

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Posted November 16, 2018.
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Genomic analysis of dingoes identifies genomic regions under reversible selection during domestication and feralization
Shao-jie Zhang, Guo-Dong Wang, Pengcheng Ma, Liang-liang Zhang, Ting-Ting Yin, Yan-hu Liu, Newton O. Otecko, Meng Wang, Ya-ping Ma, Lu Wang, Bingyu Mao, Peter Savolainen, Ya-ping Zhang
bioRxiv 472084; doi: https://doi.org/10.1101/472084
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Genomic analysis of dingoes identifies genomic regions under reversible selection during domestication and feralization
Shao-jie Zhang, Guo-Dong Wang, Pengcheng Ma, Liang-liang Zhang, Ting-Ting Yin, Yan-hu Liu, Newton O. Otecko, Meng Wang, Ya-ping Ma, Lu Wang, Bingyu Mao, Peter Savolainen, Ya-ping Zhang
bioRxiv 472084; doi: https://doi.org/10.1101/472084

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