Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

Genome Research

Volumn 26, Issue 1, 2016, Pages 1-11

  Li, Gang ^a   Davis, Brian W ^a,b,d   Eizirik, Eduardo ^c   Murphy, William J ^a,b  

^a TEXAS A AND M UNIVERSITY   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CAT BREED; COMPARATIVE STUDY; CONTROLLED STUDY; DOMESTIC CAT; FELIS LYBICA; FEMALE; GENE FLOW; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME ANALYSIS; GENOTYPE; MALE; MITOCHONDRIAL GENOME; MOLECULAR HYBRIDIZATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PANTHERA; PHYLOGENOMICS; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEX DIFFERENCE; SPECIES COMPARISON; SPECIES DIFFERENCE; SPECIES DIVERSITY; TIME PERCEPTION; X CHROMOSOME; Y CHROMOSOME; ANIMAL; CAT; CHROMOSOME; FELIDAE; GENETIC ASSOCIATION STUDY; GENETIC VARIATION; GENETICS; GENOTYPING TECHNIQUE; HYBRIDIZATION; PHYLOGENY; SEX CHROMOSOME; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION;

ANIMALS; CATS; CHROMOSOMES, MAMMALIAN; FELIDAE; FEMALE; GENE FLOW; GENETIC ASSOCIATION STUDIES; GENETIC SPECIATION; GENETIC VARIATION; GENOME, MITOCHONDRIAL; GENOTYPING TECHNIQUES; HYBRIDIZATION, GENETIC; MALE; PHYLOGENY; POLYMORPHISM, SINGLE NUCLEOTIDE; SEQUENCE ALIGNMENT; SEX CHROMOSOMES;

EID: 84956706739     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.186668.114     Document Type: Article

References (72)

1. Ai H, Fang X, Yang B, Huang Z, Chen H, Mao L, Zhang F, Zhang L, Cui L, He W, et al. 2015. Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. N at Genet 47: 217-225.
2. Ali SS, Yu Y, Pfosser M, Wetschnig W. 2012. Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP ( Reconstruct Ancestral State in Phylogenies). Ann Bot 109: 95-107.
3. AllendorfFW, Leary RF, Spruell P, Wenburg JK. 2001. The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16: 613-622.
4. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, MillerW, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Antunes A, Pontius J, Ramos MJ, O'Brien SJ, Johnson WE. 2007. Mitochondrial introgressions into the nuclear genome of the domestic cat. J Hered 98: 414-420.
6. Buckley- Beason VA, Johnson WE, Nash WG, Stanyon R, Menninger JC, Driscoll CA, Howard J, Bush M, Page JE, Roelke ME, et al. 2006. Molecular evidence for species-level distinctions in clouded leopards. Curr Biol 16: 2371-2376.
7. Cahill JA, Green RE, Fulton TL, Stiller M, Jay F, Ovsyanikov N, Salamzade R, St John J, Stirling I, Slatkin M, et al. 2013. Genomic evidence for island population conversion resolves conflicting theories of polar bear evolution. PLoS Genet 9: e1003345.
8. Cahill JA, Stirling I, Kistler L, Salamzade R, Ersmark E, Fulton TL, Stiller M, Green RE, Shapiro B. 2014. Genomic evidence of geographically widespread effect of gene flow from polar bears into brown bears. Mol Ecol 24: 1205-1217.
9. Charlesworth B, Coyne JA, Barton NH. 1987. The relative rates of evolution of sex-chromosomes and autosomes. Am Nat 130: 113-146.
10. Cho YS, Hu L, Hou HL, Lee H, Xu JH, Kwon S, Oh S, Kim HM, Jho S, Kim S, et al. 2013. The tiger genome and comparative analysis with lion and snow leopard genomes. Nat Commun 4: 2433.
11. Cui R, Schumer M, Kruesi K, Walter R, Andolfatto P, Rosenthal GG. 2013. Phylogenomics reveals extensive reticulate evolution in Xiphophorus fishes. Evolution 67: 2166-2179.
12. Currat M, Ruedi M, Petit RJ, Excoffier L. 2008. The hidden side of invasions: massive introgression by local genes. Evolution 62: 1908-1920.
13. Davis BW,Raudsepp T,Pearks Wilkerson AJ,Agarwala R,Schäffer AA,Houck M,Chowdhary BP,Murphy WJ. 2009 A high-resolution cat radiation hybrid and integrated FISH mapping resource for phylogenomic studies acr oss Felidae Genomics 93 299-304.
14. Davis BW, Li G, Murphy WJ. 2010. Supermatrix and species tree methods resolve phylogenetic relationships within the big cats, Panthera (Carnivora: Felidae). Mol Phylogen Evol 56: 64-76.
15. Davis BW, Seabury CM, Brashear W, Li G, Roelke-Parker M, Murphy WJ. 2015. M echanisms underlying mammalian hybrid sterility in two feline interspecies models. Mol Biol Evol 32: 2534-2546.
16. Decker JE, Pires JC, Conant GC, Mckay SD, Heaton MP, Chen KF, Cooper A, Vilkki J, Seabury CM, Caet ano AR, et al. 2009. Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci 106: 18644-18649.
17. Durand EY, Patterson N, Reich D, Slatkin M. 2011. Testing for ancient admixture between closely related populations. Mol Biol Evol 28: 2239-2252.
18. Eaton DA, Ree RH. 2013. Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Syst Biol 62: 689-706.
19. Eizirik E, Yuhki N, Johnson WE, Menotti-Raymond M, Hannah SS, O'Brien SJ. 2003. Molecular genetics and evolution of melanism in the cat family. Curr Biol 13: 448-453.
20. Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, Künstner A, Mäkinen H, Nadachowska-Brzyska K, Qvarnströ m A, et al. 2012. The genomic landscape of species divergence in Ficedula flycatchers. Nature 491: 756-760.
21. Garrigan D, Kingan SB, Geneva AJ, Andolfatto P, Clark AG, Thornton KR, Presgraves DC. 2012. Genome sequencing reveals complex speciation in the Drosophila simulans clade. Genome Res 22: 1499-1511.
22. Good JM, Hird S, Reid N, Demboski JR, Steppan SJ, Martin-Nims TR, Sullivan J. 2008. Ancient hybridization and mitoch ondrial capture between two species of chipmunks. Mol Ecol 17: 1313-1327.
23. Gray AP. 1972. Mammalian hybrids, a check-list and bibliography, rev. ed. Commonwealth Agricultural Bureaux, Bucks, England.
24. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, et al. 2010. A draft sequence of the Neandertal genome. Science 328: 710-722.
25. Haldane JBS. 1922. Sex ratio and unisexual sterility in hybrid animals. J Genet 12: 101-109.
26. Haq BU, Hardenbol J, Vail PR. 1987. Chronology of fluctuating sea levels since the Triassic. Science 235: 1156-1167.
27. Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42: 182-192.
28. Hobolth A, Christensen OF, Mailund T, Schierup MH. 2007. Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model. PLoS Genet 3: e7.
29. Hobolth A, Dutheil JY, Hawks J, Schierup MH, Mailund T. 2011. Incomplete lineage sorting patterns among human, chimpanzee, and orangutan suggest recent orangutan speciation and widespread selection. Genome Res 21: 349-356.
30. Homyack JA, Vashon JH, Libby C, Lindquist EL, Loch S, McAlpine DF, Pilgrim KL, Schwartz MK. 2008. Canada lynx-bobcat (Lynx canadensis × L. rufus) hybrids at the southern periphery of lynx ran ge in Maine, Minnesota and New Brunswick. Am Mid Nat 159: 504-508.
31. Johnson WE, Slattery JP, Eizirik E, Kim JH, Raymond MM, Bonacic C, Cambre R, Crawshaw P, Nunes A, Seuanez HN, et al. 1999. Disparate phylogeographic patterns of molecular genetic variation in four closely related South American small cat species. Mol Ecol 8: S79-S94.
32. Johnson WE, Eizirik E, Pecon-Slattery J, Murphy WJ , Antunes A, Teeling E, O'Brien SJ. 2006. The late Miocene radiation of modern Felidae: a genetic assessment. Science 311: 73-77.
33. Jones CS, Tegelstrom H, Latchman DS, Berry RJ. 1988. An improved rapid method for mitochondrial DNA isolation suitable for use in the study of closely related populations. Biochem Genet 26: 83-88.
34. Katoh K, Toh H. 2010. Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26: 1899- 1900.
35. Khan FAA,Phillips CD,Baker RJ 2014 Timeframes of speciation, reticulation, and hybridization in the bulldog bat explained through phylogenetic analyses of all genetic transmission elements. Syst Biol 63 96-110
36. Koen EL, Bowman J, Lalor JL, Wilson DE. 2014. Continental-scale assessment of the hybrid zone between bobcat and Canada lynx. Biol Conserv 178: 107-115.
37. Koufos GD, Kostopoulos DS, Vlachou TD. 2005. Neogene/Quaternary mammalian migrations in Eastern Mediterranean. Belgian J Zool 135: 181-190.
38. Kutschera VE, Bidon T, Hailer F, Rodi JL, Fain SR, Janke A. 2014. Bears in a forest of gene trees: Phylogenetic inference is complicated by incomplete lineage sorting and gene flow. Mol Biol Evol 31: 2004-2017.
39. Le Roux JJ, Foxcroft LC, Herbs t M, MacFadyen S. 2015. Genetic analysis shows low levels of hybridization between African wildcats (Felis silvestris lybica) and domestic cats (F. s.catus) in South Africa. Ecol Evol 5: 288-299.
40. Li H, Durbin R . 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
41. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G , Durbin R, Proc GPD. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
42. Li G, Janecka JE, Murphy WJ. 2011. Accelerated evolution of CES7, a gene encoding a novel major urinary protein in the cat family. Mol Biol Evol 28: 911-920.
43. Luo R, Liu B, Xie Y, Li Z, Huang W, Yuan J, He G, Chen Y, Pan Q, Liu Y, et al. 2012. SOAPdenovo2: an empirically improved memory-efficient shortread de novo assembler. Gigascience 1: 18.
44. Luo SJ, Zhang Y, Johnson W E, Miao L, Martelli P, Antunes A, Smith JL, O'Brien SJ. 2014. Sympatric Asian felid phylogeography reveals a major Indochinese-Sundaic divergence. Mol Ecol 23: 2072-2092.
45. Ma J, Iannuccelli N, Duan Y, Huang W, Guo B, Riquet J, Huang L, Milan D. 2010. Recombinational landscape of porcine X chromosome and individual variation in female meiotic recombination associated with haplotypes of Chinese pigs. BMC Genomics 11: 159.
46. Martin SH, Dasmahapatra KK, Nadeau NJ, Salazar C, Walters JR, Simpson F, Blaxter M, Manica A, Mallet J, Jiggins CD. 2013. Genome-wide evidence for speciation with gene flow in Heli conius butterflies. Genome Res 23: 1817- 1828.
47. McCue ME, Bannasch DL, Petersen JL, Gurr J, Bailey E, Binns MM, Distl O, Guerin G, Hasegawa T, Hill EW, et al. 2012. A high density SNP array for the domestic horse and extant Perissodactyla: utility for association mapping, genetic diversity, and phylogeny studies. PLoS Genet 8: e1002451.
48. Montague MJ, Li G, Gandolfi B, Khan R, Aken BL, Sear le SM, Minx P, Hillier LW, Koboldt DC, Davis BW, et al. 2014. Comparative analysis of the domestic cat genome reveals genetic signatures underlying feline biology and domestication. Proc Natl Acad Sci 111: 17230-1 7235.
49. Mullikin JC, Hansen NF, Shen L, Ebling H, Donahue WF, TaoW, Saranga DJ, Brand A, Rubenfield MJ, Young AC, et al. 2010. Light whole genome sequence for SNP discovery across domestic cat bree ds. BMC Genomics 11: 406.
50. Murphy WJ, Sun S, Pecon-Slattery J, Chen ZQ, O'Brien SJ. 1999. Extensive conservation of sex chromosome organization between cat and human revealed by parallel radiation hybrid mapping. Genome Res 9: 1223-1230.
51. Nussberger B, Greminger MP, Grossen C, Keller LF, Wandeler P. 2013. Development of SNP markers identifying European wildcats, domestic cats, and their admixed prog eny. Mol Ecol Resour 13: 447-460.
52. O'Fallon B. 2013. Purifying selection causes widespread distortions of genealogical structure on the human X chromosome. Genetics 194: 485-492.
53. Patterson N, Richter DJ, Gnerre S, Lander ES, Reich D. 2006. Genetic evidence for complex speciation of humans and chimpanzees. Nature 441: 1103-1108.
54. Petit RJ, Excoffier L. 2009. Gene flow and species delimitation. Trends Ecol Evol 24: 386-393.
55. Pontius JU, Mullikin JC, Smith DR, Lindblad-Toh K, Gnerre S, Clamp M, Chang J, Stephens R, Neelam B, Volfovsky N, et al. 2007. Initial sequence and comparative analysis of the cat genome. Genome Res 17: 1675-1689.
56. Posada D,Crandall KA. 1998 MODELTEST: testing the model of DNA substitution Bioinformatics 14, 817-818.
57. Qiu ZX. 2003. Dispersals of Neogene carnivorans between Asia and North America. Bull Am Mus Nat Hist 279: 18-31.
58. Roca AL, Georgiadis N, O'Brien SJ. 2005. Cytonuclear genomic dissociation in African elephant species. Nat Genet 37: 96-100.
59. Schmidt-Kuntzel A, Nelson G, David VA, Schaffer AA, Eizirik E, Roelke ME, Kehler JS, Hannah SS, O'Brien SJ, Menotti-Raymond M. 2009. A domestic catX chromosome linkage map and the sex-linked orange locus: mapping of orange, multip le origins and epistasis over nonagouti. Genetics 181: 1411-1425.
60. Schwartz MK, Pilgrim KL, McKelvey KS, Lindquist EL, Claar JJ, Loch S, Ruggiero LF. 2004. Hybridization between Canada lynx an d bobcats: genetic results and management implications. Conserv Genet 5: 349-355.
61. Shimodaira H, Hasegawa M. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246-1247.
62. Smith JM, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res 89: 391-403.
63. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
64. Streicher JW, Devitt TJ, Goldberg CS, Malone JH, Blackmon H, Fujita MK. 2014. Diversification and asymmetrical g ene flow across time and space: lineage sorting and hybridization in polytypic barking frogs. Mol Ecol 23: 3273-3291.
65. Sullivan J, Demboski JR, Bell KC, Hird S, Sarver B, Reid N, Good JM. 2014. D ivergence with gene flow within the recent chipmunk radiation (Tamias). Heredity 113: 185-194.
66. Sunquist M, Sunquist F. 2002. Wild cats of the world. Univ. of Chicago Press, Chicago.
67. Toews DPL, Brelsford A. 2012. The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21: 3907-3930.
68. Trigo TC, Freitas TRO, Kunzler G, Cardoso L, Silva JCR, Johnson WE, O'Brien SJ , Bonatto SL, Eizirik E. 2008. Inter-species hybridization among Neotropical cats of the genus Leopardus, and evidence for an introgressive hybrid zone between L. geoffroyi and L. tigrinus in southern Brazil. Mol Ecol 17: 4317-4333.
69. Trigo TC, Schneider A, de Oliveira TG, Lehugeur LM, Silveira L, Freitas TRO, Eizirik E. 2013. Molecular data reveal complex hybridization and a cryptic species of Neotropical wild cat. Curr Biol 23: 2528-2533.
70. Trigo TC, Tirelli FP, Freitas TRO, Eizirik E. 2014. Comparative assessment of genetic and morphological variation at an extensive hybrid zone between two wild cats in southern Brazil. PLoS One 9: e108469.
71. Wurster-Hill DH, Centerwall WR. 1982. The interrelationships of chromosome-banding patterns in canids, mustelids, hyena, and felids. Cytogenet Cell Genet 34: 178-192.
72. Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.