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Home , Asiatic wildcat, Chinese mountain cat, European wildcat

2018/1/23

Domestic : the favorite pet

• Over 50 breeds certified by CFA (Cat Fanciers’ club)

Genomic Evidence for the as a Conspecific of the with Contemporary Introgression to Local Domestic

He Yu Lab of Genome Diversity and (PI: Shu-Jin Luo) School of Life Sciences, Peking University 2018.1.14

From CFA website

Wildcat ( silvestris) in

• (F. s. ornata) • Distributed in , including , , , Inner in China

Asiatic wildcat • The only spotted lineage in the wildcat F. s. ornata • Chinese mountain cat (F. s. bieti) F. s. silvestris • Endemic to China, distributed in , Qinghai and Gansu • Controversial status • of the wildcat: based on genetic information (Driscoll, 2007) • Independent : based on morphology and biogeography study (Kitchener, 2009) Chinese mountain cat F. s. bieti F. s. lybica South African wildcat F. s. cafra Modified based on “Cats in China”

Domestic cats in China Inter-taxa hybridization in felids

• Literature and historical records • Commonly observed in various lineages • The book of songs: 3000 years ago • Trigo, 2013: the lineage • Wild? Domestic? • Li, 2016: , Felis, and • Origin of Chinese domestic cats Leopardus lineages • From Persis through the Silk Road (Han Dynasty, ~2000 yBPs) • Hybridization between domestic cats and • Genetic background of Chinese domestic cats European wildcats • Lack of systematic studies • Studied for decades (Randi 2001, Beaumont • Genetic relationship with local wildcats 2001, Lecis 2006, etc) Trigo, 2013 • Hybridization between domestic cats and wildcats in China?

Li, 2016

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Genetic studies of cat domestication Objectives

• Driscoll, 2007: the first • Have wildcats native to China involved in the establishment of comprehensive genetic study Chinese domestic cat population, which can be detected in the of cat domestication genome of present Chinese domestic cats? • 979 domestic and wild cats • Genomic background of Chinese domestic cats and wildcats • MtDNA and STR markers • Contribution of wildcat lineages to the gene pool of Chinese domestic cats • Near Eastern origin of the domestic cat from F. s. lybica Driscoll, 2007 • Is the Chinese mountain cat an independent species or a conspecific • Ottoni, 2017: cat dispersal of the wildcat? pattern based on ancient DNA • Phylogeny and demographic history of the Chinese mountain cat • 352 ancient cats from western Asia, and Africa • Genetic interaction with the Asiatic wildcat and domestic cats • Nine mtDNA fragments • Near East & Egypt

• No sample from East Asia

Ottoni, 2017

Domestic cats (N = 238) Wildcats (N = 11 + 1) Project outline

Sample collection • Outbreed domestic cats in China (Buccal swabs • Wildcats from institutes and the wild (Bloods, and boods) tissues, feces, etc)

DNA extraction

Multi-locus sequencing • MtDNA and Y-chromosome haplotypes • Preliminary genetic background

Representative individuals

Mitogenome sequencing • Library construction and next generation • Phylogenetic analysis sequencing

High-quality individuals

Whole genome resequencing • Population structure, phylogeny, gene flow and demography history analysis Taxonomy Sampling individual Mt sequenced Ychr sequenced Mitogenome Nuclear genome Domestic cat 238 234 83 54 46 Chinese mountain cat 11 11 5 8 4 Asiatic wildcat 1 1 1 1 1

Mt and Ychr fragment topology Next generation sequencing • MtDNA fragment: 106 variable sites in 2620bp (ND5, ND6, CytB) Mitochondrial Genome Nuclear Genome • 44 domestic cat haplotypes, six wildcat haplotypes • 77 individuals • 73 individuals • Ychr fragment: six variable sites in • 46 Chinese domestic cats • 46 Chinese domestic cats 1015bp (DBY7, SMCY7) • 20 worldwide domestic cats • 20 worldwide domestic cats • Three haplotypes correlated with three • Eight Chinese mountain cats • Four Chinese mountain cats subspecies • One Asiatic wildcat • One Asiatic wildcat • Two black-footed cats • Two black-footed cats Admixture between lineages • 70 mitogenome haplotypes • Mean coverage: 7.75-15.07 • ~ 20 million SNPs • Chinese mountain cat & Asiatic wildcat • 4/11 Chinese mountain cats with mtDNA • Data analysis • Data analysis haplotype in “ornata” cluster • Phylogenetic analysis • Phylogenetic analysis • Wide distribution: ancient admixture • TMRCA estimation • Population structure between the lineages • Gene flow • Chinese mountain cat & domestic cat • Demographic history • Three domestic cats with Ychr haplotype as “bieti” • Sympatric distribution: recent hybridization?

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Phylogeny Principal Component Analysis

Eigenvector Eigenvalue TW Statistic P-value Percentage (%) 1 26.35 8.605 4.05E-09 36.10 2 7.33 21.624 5.03E-31 10.04 3 3.37 25.159 1.83E-38 4.62 4 2.59 33.696 1.37E-58 3.54 5 1.24 12.106 4.82E-14 1.70

• PC1: black-footed cat and all the others, species level differentiation • Discordance between autosomal, Mitogenome and Y-chromosome phylogenies • PC2: Chinese mountain cat, Asiatic wild cat and domestic cat, subspecies level differentiation • No admixture in the autosomal phylogeny tree • PC3: Variance within domestic cats, difference between Chinese and worldwide domestic cats • The Chinese mountain cat located within the domestic cat clade

Introgression from Chinese mountain cats to domestic cats Population structure and Pairwise FST Qinghai

Sichuan

F. nigripes F. s. bieti F. s. ornata F. catus (Chinese) F. catus (Worldwide) F. nigripes 0 0.938 0.926 0.829 0.796 F. s. bieti 0.938 0 0.758 0.613 0.558 F. s. ornata 0.926 0.758 0 0.574 0.51 F. catus (Chinese) 0.829 0.613 0.574 0 0.116 F. catus (Worldwide) 0.796 0.558 0.51 0.116 0 • Introgression from Chinese mountain cats to sympatric Chinese domestic cats • Comparable divergence level between Chinese mountain cat, Asiatic wildcat and domestic cat

Timing of the hybridization event Demography history inferred from PSMC

• Spatial distribution of “Bieti” ancestry alleles • Different introgression regions between individuals • Large introgression segments around 30-50 Mb

• Timing of hybridization with Alder • Around 14 generations (~30 years) • Ongoing admixture process between Chinese mountain cats and sympatric domestic cats

• Chinese mountain cat and Asiatic • Domestic cat (and African wildcat) wildcat • 0.4~0.1 Mya: population expansion • 2~1 Mya: moderate expansion • 0.1 Mya ~ recent: population decline • 1 Mya ~ recent: population decline • Discordance between 10kya~0.1Mya: admixture with European wildcat?

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Demography history inferred from G-PhoCS Demography history inferred from G-PhoCS

• Four groups • Split time and population size • Domestic cat (3 candidates) • ~ 1.8 Mya: divergence between catus/lybica lineage and bieti/ornata lineage • Chinese mountain cat (4 • ~ 1.2 Mya: divergence between bieti and ornata candidates) • Gene flow events • Asiatic wildcat • bieti/ornata --> • Black-footed cat catus/lybica • Four migration bands • Catus/lybica --> • Catus --> bieti ornata • Catus --> ornata • Ornata --> bieti • Ornata --> bieti • Catus --> bieti • Wildcat --> catus

Demography history inferred from G-PhoCS Conclusions

• Split time and population size • Chinese mountain cat as a subspecies of the wildcat (Felis silvestris • ~ 1.8 Mya: divergence between catus/lybica lineage and bieti/ornata lineage bieti) • ~ 1.2 Mya: divergence between bieti and ornata • Located within the domestic cat clade in phylogenetic analysis • Subspecies-level genetic differentiation with the Asiatic wildcat and domestic • Gene flow events cats • bieti/ornata --> catus/lybica • Catus/lybica --> • Chinese domestic cats originated from the African wildcat ornata • Indifferent with worldwide domestic cats in most areas of China • Ornata --> bieti • Recent introgression from the Chinese mountain cat detected in Sichuan and • Catus --> bieti Qinghai

• Complex hybridization scenario among wildcat lineages • Ancient introgression from the Asiatic wildcat to the Chinese mountain cat • Contemporary introgression from the Chinese mountain cat to sympatric domestic cats

Acknowledgements

• Dr. Shu-Jin Luo • At Luolab: Yueting Xing, Hao Meng, Dr. Xiao Xu, Huaiqng Chen, Yan Zhuang, Dr. Lin Miao, Yuechen Liu • In the field: Bing He, Yanlin Liu, Sheng Li, Cheng Wen, Zhouba, Kewei Jiang, Jiangping Huang, Pan Zhang, Jinfan Wang, Yaoxing Su, Bo Jin, Yongping He • Sample coordination: Northwest Institute of Plateau Biology, CAS (Xining, China), Xining Zoo (Xining, China), Gansu Endangered Protection Center (Wuwei, China) • International cooperation: Stephen O’Brien, Marilyn Raymond (NCI, USA), Nobuyuki Yamaguchi (Qatar University), Carlos Driscoll (NIAAA, USA) • School of Life Sciences in Peking University, Peking-Tsinghua-NIBS (PTN) program and Center for Life Sciences (CLS) • All the cat owners

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