The Effect of Extirpation and Reintroduction on Genetic Variability of the Gray Wolf
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1 The Effect of Extirpation and Reintroduction on Genetic Variability of the Gray Wolf B. vonholdt, D. Stahler, D. Earl, D. Smith, J. Pollinger and R. K. Wayne Ecology and Evolutionary Biology, University of California, Los Angeles
2 TALK OUTLINE I) Introduction A) Relationships & genetic diversity 1. High gene flow but ecology matters II) Extinct wolves: historic wolves of the West A) Loss of genetic variation and relationships B) Population size III) Natural and human assisted reintroduction A) Yellowstone Natural Park 1. Genealogical reconstruction 2. Levels of variation and inbreeding
3 NJ coyote s substitutions/site Crufus388 la4 la13 wolves lu33 la14 la11 la2 la10 la3 la5 la7 la1 la6 la12 la9 CSI CAU la8 lu1 lu17 lu26 lu23 lu2 lu3 lu14 lu21 lu30 lu13 lu24 lu15 lu16 lu25 lu31 lu7 lu10 lu11 lu12 lu29 lu5 lu34 lu6 lu18 lu19 lu20 lu22 lu4 lu8 lu9 lu28 lu32 lu33 lu27 Mexican wolf RELATIONSHIPS Vila et al., Mol. Ecol., 1999
4 TYPICAL SPECIES LARGE CARNIVORES 10 Nm Distance (Km) Several subspecies Few subspecies
5 Ecology Matters!! Geffen et al., 2004
6 Distance Based Redundancy analysis (dbrda) Marginal tests Variable set F P %var Fst (microsatellite) Distance Fst (mtdna RFLP) Distance Anderson and Legendre, 1999
7 Ecological Imprinting Dispersal Cervus elaphus Alces gigas X X Rangifer tarandus
8 Genetically Defined Ecotypes Carmichael et al Carmichael, 2006
9 The Great Extermination: Historic wolves of The American West Leonard et al., 2005
10 occidentalis arctos lycaon nubilis baileyi
11 Genetic Variation Historic wolves have about three times the variation of modern wolves (θ of vs 0.010) and at least 43% of the variation has been lost. White -extant Black - historic only Red -Mexican wolf Samp le Haplotype Subsp ecies Localit y JAL 471 lu33 C.l. baileyi Sierra Madre, Chihua hua, Mexico JAL 473 lu33 C.l. baileyi Colonia Garcia, Chihuahua, Mexico JAL 474 lu60 C.l. baileyi Colonia Juarez, Chihuahua, Mexico JAL 475 lu32 C.l. baileyi Tanks, Ari zona JAL 476 lu33 C.l. baileyi Ft. Bowie, Arizona JAL 477 lu47 C.l. baileyi Fort Massachuse tts, New Mexico JAL 478 lu32 C.l. baileyi Fort Massachuse tts, New Mexico JAL 545 lu33 C.l. baileyi Cloverdale, New Mexico JAL 515 lu32 C.l.nub ilus Platt River, Colorado JAL 516 lu48 C.l.nub ilus Bent County, Colorado JAL 517 lu38 C.l.nub ilus Kansas JAL 518 lu28 C.l.nub ilus Fort Hark er, Kansas JAL 519 lu49 C.l.nub ilus Grove City, Kansas JAL 520 lu38 C.l.nub ilus Grove City, Kansas JAL 521 lu50 C.l.nub ilus Fort Kearny, Nebraska JAL 522 lu28 C.l.nub ilus Fort Kearny, Nebraska JAL 523 lu38 C.l.nub ilus Platt River, Nebraska JAL 524 lu50 C.l.nub ilus Guyo Canyon, New Mexico JAL 525 lu28 C.l.nub ilus Santa Rosa, New Mexico JAL 526 lu50 C.l.nub ilus Santa Rosa, New Mexico JAL 527 lu51 C.l.nub ilus Carthage, New Mexico JAL 528 lu28 C.l.nub ilus Medora, North Dakota JAL 529 lu50 C.l.nub ilus Witchita Forest Reserve, Oklahoma JAL 530 lu52 C.l.nub ilus Afton, Oklahoma JAL 539 lu50 C.l.nub ilus Haynes, New Mexico JAL 540 lu28 C.l.nub ilus La Sol, Utah JAL 541 lu50 C.l.nub ilus Box Elder County, Utah JAL 542 lu53 C.l.nub ilus Heart Draw, Utah JAL 543 lu28 C.l.nub ilus Laramie, Wyom ing JAL 544 lu28 C.l.nub ilus Wagon Creek, Wyoming JAL 480 lu32 C.l.nub ilus Porcup ine, Labrado r JAL 557 lu54 C.l.nub ilus Labrad or Peninsula JAL 558 lu32 C.l.nub ilus Labrad or Peninsula JAL 559 lu54 C.l.nub ilus Labrad or Peninsula
12 100 --Eurasian wolves --NA wolves * Historic wolves *Extant NA wolves 1 change lu53 lu32 lu54 61 IWC * IWA 59 IWB lu61 59 lu1 lu17 lu26 lu23 lu30 lu31 lu22 lu8 lu9 lu37 lu12 * lu29 72* lu7 60 lu10 lu11 91 lu28 * lu52 * * lu38 lu48 * * * lu49 * * * * * * IWD * * lu2 lu3 lu14 lu21 54 lu15 lu13 lu24 lu5 53 lu16 lu18 84 lu19 lu20 59 lu33 52 lu4 lu * * HWD HWA HWC HWE lu6 lu34 lu47 la11 lu60 lu25 * HWB * Mexican wolf lu50 lu51 * Southern clade
13 Genetic Variation White -extant Black - historic only Red -Mexican wolf Clade (lu 33, 47,50,51) Sample Haplotype Subspecies Localit y JAL 471 lu33 C.l. baileyi Sierra Madre, Chihuahua, Mexico JAL 473 lu33 C.l. baileyi Colonia Garcia, Chihuahua, Mex ico JAL 474 lu60 C.l. baileyi Colonia Juarez, Chihuahua, Mexico JAL 475 lu32 C.l. baileyi Tanks, Arizona JAL 476 lu33 C.l. baileyi Ft. B owie, Arizona JAL 477 lu47 C.l. baileyi Fort Massachusetts, New Mexico JAL 478 lu32 C.l. baileyi Fort Massachusetts, New Mexico JAL 545 lu33 C.l. baileyi Cloverdale, Ne w Mexico JAL 515 lu32 C.l.nubilus Platt River, Colorado JAL 516 lu48 C.l.nubilus Bent County, Colorado JAL 517 lu38 C.l.nubilus Kansas JAL 518 lu28 C.l.nubilus Fort Harker, Kansas JAL 519 lu49 C.l.nubilus Grove City, Kansas JAL 520 lu38 C.l.nubilus Grove City, Kansas JAL 521 lu50 C.l.nubilus Fort Kearny, Nebraska JAL 522 lu28 C.l.nubilus Fort Kearny, Nebraska JAL 523 lu38 C.l.nubilus Platt River, Nebraska JAL 524 lu50 C.l.nubilus Guyo Canyo n, New Mexico JAL 525 lu28 C.l.nubilus Santa Rosa, N ew Mexico JAL 526 lu50 C.l.nubilus Santa Rosa, N ew Mexico JAL 527 lu51 C.l.nubilus Carthage, Ne w Mexico JAL 528 lu28 C.l.nubilus Medora, North Dakota JAL 529 lu50 C.l.nubilus Witchita Forest Reserve, Oklahoma JAL 530 lu52 C.l.nubilus Afton, Oklahoma JAL 539 lu50 C.l.nubilus Haynes, New Mexico JAL 540 lu28 C.l.nubilus La Sol, Utah JAL 541 lu50 C.l.nubilus Box Elder County, Utah JAL 542 lu53 C.l.nubilus Heart Draw, Utah JAL 543 lu28 C.l.nubilus Laramie, Wyoming JAL 544 lu28 C.l.nubilus Wagon Creek, Wyoming JAL 480 lu32 C.l.nubilus Porcupine, Labrado r JAL 557 lu54 C.l.nubilus Labrador Peninsula JAL 558 lu32 C.l.nubilus Labrador Peninsula JAL 559 lu54 C.l.nubilus Labrador Peninsula Nebraska Oklahoma Utah
14 NJ coyotes substitutions/site Crufus388 la4 la13 wolves lu33 la14 la11 la2 la10 la3 la5 la7 la1 la6 la12 la9 CSI CAU la8 lu1 lu17 lu26 lu23 lu2 lu3 lu14 lu21 lu30 lu13 lu24 lu15 lu16 lu25 lu31 lu7 lu10 lu11 lu12 lu29 lu5 lu34 lu6 lu18 lu19 lu20 lu22 lu4 lu8 lu9 lu28 lu32 lu27 Genetic Variation & population size value of θ of implies a population size of 840,000 wolves (assuming 60% of adults reproduce, 50% of the population is adult and a 3 year generation time) Vila et al., Mol. Ecol., 1999, Leonard et al., 2005
15 Consider recovery involving both ecotypes over a large area N>300 N>700
16 Yellowstone Wolf Recovery Abundant prey populations and protection led to rapid recovery
17 The Trophic Cascade
18 Yellowstone National Park Reintroduction event 1995: 14 wolves from Hinton, Alberta 1996: 17 wolves from Fort St. John, B.C. Genetic Analysis 30 canid microsatellite markers Sample collection (N = 344) mostly blood/tissue samples; serum, hair, teeth and scat Pedigree construction (N>200) Parentage analysis, relatedness simulation, observational pedigree likelihood estimation Bridgett vonholdt Dan Stahler
19 Pedigree Example: the Druid Peak pack since its establishment in 1996 Assembly rules for reintroduction Pack size = 6; Number of breeding individuals = 0
20 Druid Peak pack 1997 Pack size = 10; Number of breeding individuals = 3
21 Druid Peak pack 1998 Pack size = 10; Number of breeding individuals = 2
22 Druid Peak pack 1999 Pack size = 9; Number of breeding individuals = 2
23 Druid Peak pack 2000 Pack size = 18; Number of breeding individuals = 4
24 Druid Peak pack 2001 Pack size = 18; Number of breeding individuals = 4
25 Pack size = 18; Number of breeding individuals = 4 Druid Peak pack 2002 Pack splitting
26 Druid Peak pack 2003 Pack splitting events Pack size = 16 Number of breeding individuals = 4
27 Druid Peak pack 2004 Pack size = 14 Number of breeding individuals = 4
28 Pedigree of eleven wolf packs Assembly rules for reintroduction
29 Reintroduction Genetics Bensch et al. 2006
30 No apparent difference in the distribution of heterozygosity of F IS Proportion observed Breeding Population Nonbreeding Population Heterozygosity Heterozygosity Breeding Nonbreeding Mean Std Error Median Mode Std Deviation Sample Variance Kurtosis Skewness N F IS
31 Heterozygosity compared annually among breeding status Heterozygosity Non-breeding population Breeding population Year
32 Litter size and inbreeding No relationship between F and litter size y = x R 2 adj = n =45 observed high count litter size during den emergence period inbreeding coefficient (F) of the pups
33 Pup survival and inbreeding No relationship between F and pup survival proportion of pups in litter surviving until winter y = x R 2 adj = n = inbreeding coefficient (F) of the pups
34 Observed and predicted heterozygosity Predicted heterozygosity Observed heterozygosity N e estimates from SPARKS and PM2000
35 Annual observed F IS and predicted F Inbreeding Year Projected FIS FIS observed
36 Heterozygosity of the adult breeding pools Observed Heterozygosity Observed Random Managed Year Mate Suitability Index (MSI) = increase genetic diversity, decreases mean kinship, minimize inbreeding and exclude unknown lineages, MateRx
37 Black and White matings more common that pure colors (negative assortative mating) MALES KK Kk kk FEMALES KK 0 (0) 0 (0) 0 (0) 0 Kk 0 (0) 7 (13) 31 (25) 38 kk 0 (0) 48 (42) 70 (76) pvalue =
38 CONCLUSIONS 1) The American West once contained a genetically diverse populations of wolves, numbering > 700,000 individuals. 2) Reintroduction should involve a large area and more individuals than planned of both wolf ecotypes to their appropriate environments. Mixing of ecotypes is not bad. 3) Large scale reintroductions such as occurred in Yellowstone even if highly isolated, can preserve variation and avoid inbreeding over the short term. 4) Long term preservation should involve gene flow.
39 Acknowledgements Yellowstone National Park, NPS Dr. Steve Fain, USFWS Forensics Lab, Ashland, OR Ed Bangs; USFWS MT Carter Niemeyer, USFWS ID Joe Fontaine, USFWS MT Roger Stradley (pilot), Gallatin Flying Services, MT Yellowstone Park Foundation Nez Perce Tribe, ID Deb Guernsey, Rick McIntyre, and numerous Yellowstone Wolf Project field technicians Photography provided by: Dan Stahler/NPS, Bridgett vonholdt and Carl Swaboda
40 Annual population F IS Population N FIS Predicted ~ Year Population N FIS
41 Annual population heterozygosity Population N Heterozygosity Predicted ~ Year Population N Heterozygosity
42 Differential Survivorship
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