Genome-wide signatures of population bottlenecks and diversifying selection in European wolves

Heredity

Volumn 112, Issue 4, 2014, Pages 428-442

  Pilot, M ^a,b   Greco, C ^c   Vonholdt, B M ^d   Jedrzejewska B ^e   Randi, E ^c,f   Jedrzejewski W ^e,i   Sidorovich, V E ^g   Ostrander, E A ^h   Wayne, R K ^d  

^a UNIVERSITY OF LINCOLN   (United Kingdom)

^b MUSEUM AND INSTITUTE OF ZOOLOGY   (Poland)

^c INSTITUTE FOR ENVIRONMENTAL PROTECTION AND RESEARCH ISPRA   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e MAMMAL RESEARCH INSTITUTE   (Poland)

^f AALBORG UNIVERSITY   (Denmark)

^g INSTITUTE OF ZOOLOGY   (Belarus)

^h NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

ⁱ INSTITUTO VENEZOLANO DE INVESTIGACIONES CIENTÍFICAS   (Venezuela)

Author keywords

bottleneck; effective population size; genetic differentiation; grey wolf; linkage disequilibrium; selection

Indexed keywords

BODY SIZE; CANID; DISEQUILIBRIUM; DIVERGENCE; DOMESTICATION; EFFECTIVE POPULATION SIZE; EVOLUTIONARY BIOLOGY; GENETIC DIFFERENTIATION; GENETIC DRIFT; GENOME; GENOMICS; GROWTH RATE; PLEISTOCENE; POPULATION BOTTLENECK;

EASTERN EUROPE; IBERIAN PENINSULA; ITALY;

CANIDAE;

ANIMAL; CLASSIFICATION; EASTERN EUROPE; GENETIC DRIFT; GENETIC VARIABILITY; GENETICS; ITALY; POPULATION GENETICS; PRINCIPAL COMPONENT ANALYSIS; SPAIN; WOLF; X CHROMOSOME;

ANIMALS; EUROPE, EASTERN; GENETIC DRIFT; GENETIC VARIATION; GENETICS, POPULATION; ITALY; PRINCIPAL COMPONENT ANALYSIS; SPAIN; WOLVES; X CHROMOSOME;

EID: 84897022967     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2013.122     Document Type: Article

References (80)

1. Allendorf FW, Hohenlohe PA, Luikart G (2010). Genomics and the future of conservation genetics. Nat Rev Genet 11: 697-709
2. Alexander DH, Novembre J, Lange K (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655-1664
3. Altobello G (1921). [Fauna of Abruzzo and Molise]. Mammiferi 4: 38-45, [In Italian].
4. Alvarez RH, Kantarjian HM, Cortes JE (2006). Biology of platelet-derived growth factor and its involvement in disease. Mayo Clin Proc 81: 1241-1257
5. Axelsson E, Ratnakuma A, Arendt ML, Maqbool K, Webster MT, Perloski M et al. (2013). The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495: 360-364
6. Barja I (2009). Prey and prey-Age preference by the Iberian wolf Canis lupus signatus in a multiple-prey ecosystem. Wildlife Biol 15: 147-154
7. Bassem MD, Lars S (2011). Regulation of human adipose-derived stromal cell osteogenic differentiation by insulin-like growth factor-1 and platelet-derived growth factor-Alpha. Plast Reconstr Surg 127: 1022-1023
8. Beaumont MA, Balding DJ (2004). Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol 13: 969-980
9. Bocquet-Appel JP (2011). When the world's population took off: The springboard of the Neolithic Demographic Transition. Science 333: 560-561
10. Boitani L (2003). Wolf conservation and recovery. In Mech LD, Boitani L (eds). Wolves: Behavior, Ecology, and Conservation. The University of Chicago Press: Chicago 317-340
11. Boyko AR, Quignon P, Li L, Schoenebeck J, Degenhardt JD, Lohmueller KE et al. (2010). A simple genetic architecture underlies quantitative traits in dogs. PLoS Biol 8: E1000451
12. Cabrera A (1907). Los lobos De Espana. Bol R Soc Esp Hist Nat 7: 193-198
13. Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Feled-Alon A, York TL et al. (2007). Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3: E163
14. Czarnomska SD, Jédrzejewska B, Borowik T, Niedzialkowska M, Stronen AV, Nowak S et al. (2013). Concordant mitochondrial and microsatellite DNA structuring between Polish lowland and Carpathian Mountain wolves. Cons Genet 14: 573-588
15. Earl DA, vonholdt BM (2012). Structure Harvester: A website and program for visualizing structure output and implementing the Evanno method. Conserv Genet Resour 4: 359-361
16. Evanno G, Regnaut S, Goudet J (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Mol Ecol 14: 2611-2620
17. Fabbri E, Caniglia R, Kusak J, Galov A, Gomercić T, Arbanasić H et al. Genetic structure of expanding wolf (Canis lupus) populations in Italy and Croatia, and the early steps of the recolonization of the Eastern Alps. Mamm Biol (in press
18. Foll M, Gaggiotti O (2008). A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics 180: 977-993
19. Freedman AH, Schweizer RM, Gronau I, Han E, Ortega - Del Vecchyo D, Silva PM et al. Genome sequencing highlights the dynamic early history of dogs. PLoS Genet. (in press
20. Frisse L, Hudson RR, Bartoszewicz A, Wall JD, Donfack J, Di Rienzo A (2001). Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am J Hum Genet 69: 831-843
21. Gattepaille LM, Jakobsson M, Blum MG (2013). Inferring population size changes with sequence and SNP data: Lessons from human bottlenecks. Heredity 110: 409-419
22. Gautier M, Vitalis R (2013). Inferring population histories using genome-wide allele frequency data. Mol Biol Evol 30: 654-668
23. Geffen E, Anderson MJ, Wayne RK (2004). Climate and habitat barriers to dispersal in the highly mobile grey wolf. Mol Ecol 13: 2481-2490
24. Germonpré M, Sablin MV, Stevens RE, Hedges REM, Hofreiter M, Stiller M et al. (2009 Fossil dogs and wolves from Palaeolithic sites in Belgium, the Ukraine and Russia: osteometry, ancient DNA and stable isotopes. J Arch Science 36: 473-490
25. Gomercic T, Sindicic M, Galov A, Arbanasic H, Kusak J, Kocijan I et al. (2010). High genetic variability of the grey wolf (Canis lupus L.) population from Croatia as revealed by mitochondrial DNA control region sequences. Zool Stud 49: 816-823
26. Gompper ME (2002). Top carnivores in the suburbs? Ecological and conservation issues raised by colonization of north eastern North America by coyotes. Bioscience 52: 185-190
27. Gray MM, Sutter NB, Ostrander EA, Wayne RK (2010). The IGF1 small dog haplotype is derived from Middle Eastern grey wolves. BMC Biol 8: 1-13
28. Hayes BJ, Visscher PM, McPartlan HC, Goddard ME (2003). Novel multilocus measure of linkage disequilibrium to estimate past effective population size. Genome Res 13: 635-643
29. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, Cresko WA (2010). Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6: E1000862
30. Hofreiter M, Barnes I (2010). Diversity lost: Are all Holarctic large mammal species just relict populations? BMC Biol 8: 46
31. Jédrzejewska B, Jédrzejewski W, Bunevich AN, Minkowski L, Okarma H (1996). Population dynamics of wolves Canis lupus in Bialowieza primeval forest (Poland and Belarus) in relation to hunting by humans, 1847-1993. Mammal Rev 26: 103-126
32. Jédrzejewski W, Branicki W, Veit C, Mejugorac I, Pilot M, Bunevich AN et al. 2005 Genetic diversity and relatedness within packs in an intensely hunted population of wolves Canis lupus. Acta Theriol 50 3-22
33. Jédrzejewski W, Jédrzejewska B, Andersone-Lilley Z, Balciauskas L, Mannil P, Ozolins J et al. (2010). Synthesizing wolf ecology and management in Eastern Europe: Similarities and contrasts with North America. In: Musiani M, Boitani L, Paquet PC (eds). The World of Wolves. New perspectives on Ecology, Behavior and Management. University of Calgary Press: Calgary 207-233
34. Jones FC, Chan YF, Schmutz J, Grimwood J, Brady S, Southwick A et al. (2012). A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr Biol 22: 83-90
35. Kalinowski ST (2011). The computer program STRUCTURE does not reliably identify the main genetic clusters within species: Simulations and implications for human population structure. Heredity 106: 625-632
36. Keigwin LD, Donnelly JP, Cook MS, Neal W., Driscoll NW, Brigham-Grette J (2006). Rapid sea-level rise and Holocene climate in the Chukchi Sea. Geology 34: 861-864
37. Keller I, Wagner CE, Greuter L, Mwaiko S, Selz OM, Sivasundar A et al. (2013). Population genomic signatures of divergent adaptation, gene flop and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol Ecol 22: 2848-2863
38. Kijas JW, Lenstra JA, Hayes B, Boitard S, Porto Neto LR, San Cristobal M et al. (2012). Genome-wide analysis of the world's sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol 10: E1001258
39. Konovalov DA, Manning C, Henshaw MT (2004). KINGROUP: A program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol Ecol Notes 4: 779-782
40. Leonard JA, Vilà C, Fox-Dobbs K, Koch PL, Wayne RK, Van Valkenburgh B (2007). Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr Biol 17: 1146-1150
41. Lindblad-Toh K, Wade CM, Mikkelsen TS, Karlsson EK, Jaffe DB, Kamal M et al. (2005). Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803-819
42. Lucchini V, Galov A, Randi E (2004). Evidence of genetic distinction and long-term population decline in wolves (Canis lupus) in the Italian Apennines. Mol Ecol 13: 523-536
43. MacNulty DR, Smith DW, Mech LD, Eberly LE (2009). Body size and predatory performance in wolves: Is bigger better? J Anim Ecol 78: 532-539
44. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639-655
45. Mattioli L, Capitani C, Gazzola A, Scandura M, Apollonio M (2011). Prey selection and dietary response by wolves in a high-density multi-species ungulate community. Eur J Wildlife Res 57: 909-922
46. McEvoy BP, Powell JE, Goddard ME, Visscher PM (2011). Human population dispersal 'Out of Africa' estimated from linkage disequilibrium and allele frequencies of SNPs. Genome Res 21: 821-829
47. Mech LD, Seal US (1987). Premature reproductive activity in wild wolves. J Mammal 68: 871-873
48. Miller W, Schuster SC, Welch AJ, Ratan A, Bedoya-Reina OC, Zhao F et al. (2012). Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change. PNAS 109: E2382-E2390
49. Musiani M, Boitani L, Paquet P (2010). The World of Wolves: New Perspectives on Ecology, Behaviour and Management. University of Calgary Press: Calgary
50. Nowak RM (2003). Wolf evolution and taxonomy. In Mech LD, Boitani L (eds Wolves: Behavior, Ecology, and Conservation. The University of Chicago Press: Chicago 239-258
51. Nowak RM, Federoff NE (2002). The systematic status of the Italian wolf Canis lupus. Acta Theriol 47: 333-338
52. Oliver MK, Piertney SB (2012). Selection maintains MHC diversity through a natural population bottleneck. Mol Biol Evol 29: 1713-1720
53. Ozolins J, Andersone Z (2001). Status of large carnivore conservation in the Baltic States. Action plan for the conservation of wolf (Canis lupus) in Latvia. European Commission: Strasbourg, T-PVS (2001) 73: Add. 2, pp 1-32
54. Patterson N, Price AL, Reich D (2006). Population structure and eigenanalysis. PLoS Genet 2: E190
55. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Be'er E, Robinson S et al. (2012 Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21: 3403-3418
56. Pilot M, Branicki W, Jédrzejewski W, Goszczyń ski J, Jédrzejewska B, Dykyy I et al. (2010). Phylogeographic history of grey wolves in Europe. BMC Evol Biol 21: 10-104
57. Pilot M, Jédrzejewski W, Branicki W, Sidorovich VE, Jédrzejewska B, Stachura K et al. (2006). Ecological factors influence population genetic structure of European grey wolves. Mol Ecol 15: 4533-4553
58. Pritchard J, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945-959
59. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al. (2007). PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575
60. Randi E (2011). Genetics and conservation of wolves Canis lupus in Europe. Mammal Rev 41: 99-111
61. Reddi AH, Cunningham NS (1990). Bone induction by osteogenin and bone morphogenetic proteins. Biomaterials 11: 33-34
62. Sastre N (2011). Genética De La conservación: El lobo gris (Canis lupus). PhD thesis Autonomous, University of Barcelona: Spain
63. Sastre N, Vila C, Salinas M, Bologov VV, Urios V, Sanchez A et al. (2011). Signatures of demographic bottlenecks in European wolf populations. Conserv Genet 12: 701-712
64. Scheet P, Stephens M (2006). A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78: 629-644
65. Schmidt MB, Chen EH, Lynch SE (2006). A review of the effects of insulin-like growth factor and platelet derived growth factor on in vivo cartilage healing and repair. Osteoarthr Cartilage 14: 403-412
66. Sidorovich VE, Tikhomirova LL, Jédrzejewska B (2003). Wolf Canis lupus numbers, diet and damage to livestock in relation to hunting and ungulate abundance in northeastern Belarus during 1990-2000. Wildlife Biol 9: 103-111
67. Sommer R, Benecke N (2005). Late-Pleistocene and early Holocene history of canid fauna of Europe (Canidae). Mamm Biol 70: 227-241
68. Spiegelhalter DJ, Best NG, Carlin BP, Linde AVD (2002). Bayesian measures of model complexity and fit. J Roy Stat Soc B 64: 583-639
69. Spiridonov G, Spassov N (1985). Wolf-Canis lupus L., 1758. In: Botev Peshev (ed) Red Data Book of Bulgaria. Bulgarian Academy of Science: Sofia, pp 132
70. Stefani CM, Machado MA, Sallum EA, Sallum AW, Toledo S, Nociti FH Jr (2000). Plateletderived growth factor/insulin-like growth factor-1 combination and bone regeneration around implants placed into extraction sockets: A histometric study in dogs. Implant Dent 9: 126-131
71. Stronen AV, Jédrzejewska B, Pertoldi C, Demontis D, Randi E, Niedzia kowska M et al. (2013). North-south differentiation and a region of high diversity in European wolves (Canis lupus). PLoS ONE 8: E76454
72. Sutter NB, Bustamante CD, Chase K, Gray MM, Zhao K, Zhu L et al. (2007). A single IGF1 allele is a major determinant of small size in dogs. Science 316: 112-115
73. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011). MEGA5: Molecular evolutionary genetics analysis using likelihood, distance, and parsimony methods. Mol Biol Evol 28: 2731-2739
74. Tenesa A, Navarro P, Hayes BJ, Duffy DL, Clarke GM, Goddard ME et al. (2007). Recent human effective population size estimated from linkage disequilibrium. Genome Res 17: 520-526
75. Vilà C (1993). Aspectos morfologicos y ecológicos del lobo iberico Canis lupus L. PhD thesis Universidad De Barcelona: Spain
76. Vilà C, Amorim I. R, Leonard J. A, Posada D, Castroviejo J, Petrucci-Fonseca F et al. (1999). Mitochondrial DNA phylogeography and population history of the grey wolf Canis lupus. Mol Ecol 8: 2089-2103
77. vonHoldt B, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P et al. (2010 Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464: 898-902
78. Von Holdt BM, Pollinger JP, Earl DA, Knowles JC, Boyko AR, Parker H et al. 2011). A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res 21 1294-1305
79. Zhao S, Pingping Z, Dong S, Zhan X, Wu Q, Guo X et al. (2013). Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nat Genet 45: 67-71
80. Zulliger D, Schnyder E, Gugerli F (2013). Are adaptive loci transferable across genomes of related species? Outlier and environmental association analyses in Alpine Brassicaceae species. Mol Ecol 22: 1626-1639