Conservation Genetics

, Volume 6, Issue 1, pp 25–37 | Cite as

Gene flow among San Joaquin kit fox populations in a severely changed ecosystem

  • Michael K. Schwartz
  • Katherine Ralls
  • Dan F. Williams
  • Brian L. Cypher
  • Kristine L. Pilgrim
  • Robert C. Fleischer
Article

Abstract

The San Joaquin kit fox (Vulpes macrotis mutica) was once ubiquitous throughout California’s San Joaquin Valley and its surrounds. However, most of its habitat has been lost to irrigated agriculture, urban development, and oil fields. The remaining foxes are concentrated in six areas, although there are several small pockets of foxes throughout the Valley. To help conserve kit foxes, we sought an ecological understanding of the level of genetic variation remaining in these locations and the extent of gene flow among them. We collected tissue from 317 kit foxes from 8 sites and estimated genetic variability in and gene flow among sites using data from 8 polymorphic, microsatellite markers. We found no differences in both observed and expected heterozygosity between locations using Bonferonni corrected paired t-tests. We found differences in mean number of alleles per locus, even after we used Monte Carlo simulations to adjust for sample size differences. Population subdivision was low among sites (Fst=0.043), yet a matrix of pairwise Fst values was correlated with a matrix of pairwise geographic distances. An assignment test classified only 45% of the individuals to the site where they were captured. Overall, these data suggest that kit fox dispersal between locations may still maintain genetic variation throughout most of the areas we sampled.

Keywords

gene flow kit fox microsatellite population genetics Vulpes macrotis mutica 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abdo, Z, Crandall, KA, Joyce, P 2004Evaluating the performance of likelihood methods for detecting population structure and migrationMol. Ecol.13837851PubMedGoogle Scholar
  2. Allegrucci, G, Minasi, MG, Sbordoni, V 1997Patterns of gene flow and genetic structure in cave-dwelling crickets of the Tuscan endemic, Dolichopoda schiavazii (Orthoptera, Rhaphidophoridae)Heredity78665673Google Scholar
  3. Allendorf, FW, Phelps, RS 1981Use of allelic frequencies to describe population structureCan. J. Fish. Aquat. Sci.3815071514Google Scholar
  4. Archie, JW 1985Statistical analysis of heterozygosity data: independent sample comparisonsEvolution39623637Google Scholar
  5. Balestreri AN (1981) Status of the San Joaquin kit fox at Camp Roberts California. Department of Army Directorate Facilities Engineering Environmental and Natural Resources Office, HQ, 7th Infantry Division, Contract No. DAKF03-81-C736, Ft. Ord. Google Scholar
  6. Beerli, P, Felsenstein, J 2001Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approachProc. Nat. Acad. Sci.9845634568PubMedGoogle Scholar
  7. Berger, J 1990Persistence of different-sized populations, an empirical assessment of extinction in bighorn populationsConserv. Biol.49198Google Scholar
  8. Brown, JH, Kodric-Brown, A 1977Turnover rates in insular biogeography, effect of immigration on extinctionEcology58445449Google Scholar
  9. Cornuet, J, Piry, S, Luikart, G, Estoup, A, Solignac, M 1999New methods employing multilocus genotypes to select or exclude populations as origins of individualsGenetics15319892000PubMedGoogle Scholar
  10. Cypher, B,  et al. 2000Population dynamics of San Joaquin kit foxes at the Naval Petroleum Reserves in CaliforniaWildlife Monogr.145143Google Scholar
  11. Cypher, B, Frost, LN 1999Condition of San Joaquin kit foxes in urban and exurban habitatsJ. Wildlife Manage.63930938Google Scholar
  12. Davies, N, Villablanca, FX, Roderick, GK 1999Determining the source of individuals, multilocus genotyping in nonequilibrium population geneticsTrend. Ecol. Evol.141721Google Scholar
  13. Environmental Systems Research Institute Inc. (ESRI) 1997. ARC/INFO version 7.1.2. Redlands, CA. Google Scholar
  14. Fisher, R 1954Statistical Methods for Research Workers 12th ed. Oliver and BoydEdinburghUKGoogle Scholar
  15. Francisco, LV, Langston, AA, Mellersh, CS, Neal, CL, Ostrander, EA 1996A class of highly polymorphic tetranucleotide repeats for canine genetic mappingMamm. Genome7359362PubMedGoogle Scholar
  16. Frankham, R 1995Effective population size/adult population size ratios in wildlife: a reviewGenet. Res. Camb.6695106Google Scholar
  17. Fredholm, M, Wintero, AK 1995Variation of short tandem repeats with in and between species belonging to the Canidae familyMamm. Genome61118PubMedGoogle Scholar
  18. Goudet, J 1995FSTAT (Version 1.2), A computer program to calculate F-statisticsJ. Hered.86485486Google Scholar
  19. Goudet J (2000) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.1) Available from http://www.unilch/izea/softwares/fstat.html Updated from Goudet (1995).Google Scholar
  20. Goudet, J, Perrin, N, Wasser, P 2002Tests for sex-biased dispersal using bi-parentally inherited genetic markersMole. Ecol.1111031114Google Scholar
  21. Goudet, J, Raymond, M, Demeeus, T, Rousset, F 1996Testing genetic differentiation in diploid populationsGenetics14419331940PubMedGoogle Scholar
  22. Greenwood, PJ 1980Mating systems, philopatry and dispersal in birds and mammalsAnim. Behav.2811401162Google Scholar
  23. Grinnell, J, Dixon, JS, Linsdale, JM 1937Fur-bearing Mammals of CaliforniaUniversity of California PressBerkleyVol 2Google Scholar
  24. Guo, SW, Thompson, EA 1992Performing the exact test of Hardy-Weinberg proportions for multiple allelesBiometrics48361362PubMedGoogle Scholar
  25. Hedrick, PW 1999Highly variable loci and their interpretation in evolution and conservationEvolution53313318Google Scholar
  26. Koopman, ME, Cypher, BL, Scrivner, JH 2000Dispersal patterns of San Joaquin Kit Foxes (Vulpes macrotis mutica)J. Mammal.81213222Google Scholar
  27. Leberg, P 2002Estimating allelic richness: effects of sample size and bottlenecksMol. Ecol.1124452449PubMedGoogle Scholar
  28. Lugon-Moulin, N, Brunner, H, Balloux, F, Hausser, J, Goudet, J 1999Do riverine barriers, history or introgression shape the genetic structuring of a common shrew (Sorex araneus) populationHeredity83155161PubMedGoogle Scholar
  29. Luikart, G, Cornuet, JM 1999Estimating the effective number of breeders from heterozygote excess in progenyGenetics15112111216PubMedGoogle Scholar
  30. Maldonado, JE, Cotera, R, Geffen, E, Wayne, RK 1997Relationships of the endangered Mexican kit fox (Vulpes macrotis zinseri) to North American arid-land foxes based on mitochondrial DNA sequence dataSouthwest. Nat.42460470Google Scholar
  31. Manel, S, Bertier, P, Luikart, G 2002Detecting wildlife poaching: identifying the origin of individuals with Bayesian assignment tests and multilocus genotypesConserv. Biol.16650659Google Scholar
  32. Mantel, N 1967The detection of disease clustering and a generalized regression approachCancer Res.27209220PubMedGoogle Scholar
  33. Mercure, A, Ralls, K, Koepfli, KP, Wayne, RK 1993Genetic subdivision among small canids: mitochondrial DNA differentiation of swift, kit and arctic foxesEvolution4713131328Google Scholar
  34. Merriam, CH 1902Three new foxes of the kit fox and desert fox groupsProc. Biol. Soc. Wash.157374Google Scholar
  35. Mills, LS, Allendorf, FW 1996The one-migrant-per-generation rule in conservation and managementConserv. Biol.1015091518Google Scholar
  36. Mills, LS, Schwartz, MK, Tallmon, DA, Lair, KP 2003

    Measuring and interpreting connectivity for mammals in coniferous forests

    Zabel, CJAnthony, RG eds. Mammal Community Dynamics: Management and Conservation in the Coniferous Forests of Western North AmericaCambridge University PressCambridge587613
    Google Scholar
  37. Nei, M, Chakravarti, A 1977Drift variances of Fst and Gst statistics obtained from a finite number of isolated populationsTheor. Popul. Biol.11307325PubMedGoogle Scholar
  38. Newman, D, Pilson, D 1997Increased probability of extinction due to decreased genetic effective population size, experimental populations of Clarkia pulchellaEvolution51354362Google Scholar
  39. C, O’Ryan, Harley, EH, Bruford, MW, Beaumont, M, Wayne, RK, Cherry, MI 1998Microsatellite analysis of genetic diversity in fragmented South African buffalo populationsAnim. Conserv.18594Google Scholar
  40. Ostrander, EA, Sprague, GF, Rine, J 1993Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dogGenomics16207213PubMedGoogle Scholar
  41. Paetkau, D, Calvert, W, Stirling, I, Strobeck, C 1995Microsatellite analysis of population structure in Canadian polar bearsMole. Ecol.4347354Google Scholar
  42. Paetkau, D, Waits, LP, Clarkson, PL, Craighead, L, Vyse, E, Ward, R, Strobeck, C 1998Variation in genetic diversity across the range of North American brown bearsConserv. Biol.12418429Google Scholar
  43. Ralls, K, Pilgrim, K, White, PJ, Paxinos, EE, Schwartz, MK, Fleischer, RC. 2001Kinship, social relationships, and den-sharing in kit foxesJ. Mamm.82858866Google Scholar
  44. Ralls, K, White, PJ 1995Predation on San Joaquin kit foxes by larger canidsJ. Mamm.76723729Google Scholar
  45. Raymond, M, Rousset, F 1995GENEPOP (Version 1.2), population genetics software for exact tests and ecumenicismJ. Hered.83248249Google Scholar
  46. Rice, WR 1989Analyzing tables of statistical testsEvolution43223225Google Scholar
  47. Robertson, A 1965The interpretation of genotypic ratios in domestic animal populationsAnim. Prod.7319324CrossRefGoogle Scholar
  48. Saccheri, I, Kuussaari, M, Kankare, M, Vikman, P, Fortelius, W, Hanski, I 1998Inbreeding and extinction in a butterfly metapopulationNature392491494Google Scholar
  49. Scrivner JH, O’Farrell TP, Kato TT (1987) Dispersal of San Joaquin kit foxes, Vulpes macrotic mutica, on Naval Petroleum Reserve #1, Kern County, California Rep No EGG10282-2190, EG&G Energy Measurements, Goleta, CA.Google Scholar
  50. Slatkin, M 1985Gene flow and geographic structure of natural populationsScience236787792Google Scholar
  51. Slatkin, M 1995A measure of population subdivision based on microsatellite allele frequenciesGenetics139457462PubMedGoogle Scholar
  52. Smith, DA, Ralls, K, Davenport, KB, Adams, B, Maldonado, JE 2001Canine assistants for conservationistsScience291435PubMedGoogle Scholar
  53. Smith DA, Ralls K, Cypher BL, Maldonado JE (In Press) Assessment of Scat-detection dog surveys to determine kit fox distribution. Wildl. Soc. Bull.Google Scholar
  54. Spiegel LK (1996) Studies of the San Joaquin kit fox in undeveloped and oil-developed areas California Energy Commission Pub No P700-96-003 California Energy Commission Publication Unit, Sacramento.Google Scholar
  55. Steinberg, EK, Jordan, CE 1997

    Using molecular genetics to learn about the ecology of threatened species: the allure and the illusion of measuring genetic structure in natural populations

    Fiedler, PAKarieva, PM eds. Conservation Biology for the Coming DecadeChapman and HallNew York440460
    Google Scholar
  56. Stow, AJ, Sunnucks, P, Briscoe, DA, Gardner, MG 2001The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellitesMole. Ecol.10867878Google Scholar
  57. Tallmon, DT, Luikart, G, Waples, RS 2004The alluring simplicity and complex reality of genetic rescueTrend. Ecol. Evol.19489496Google Scholar
  58. US Fish and Wildlife Service (1967) Native fish and wildlife Endangered species Federal Register 32, 4001.Google Scholar
  59. US Fish and Wildlife Service (1998) Recovery plan for upland species of the San Joaquin Valley, California USFWS, Region 1, Portland, Oregon. Google Scholar
  60. Vucetich, JA, Waite, TA 2000Is one migrant per generation sufficient for the genetic management of fluctuating populationsAnim. Conserv.3261266Google Scholar
  61. Wandeler, P, Funk, SM, Largiader, R, Gloor, S, Breitenmoser, U 2003The city-fox phenomenon: genetic consequences of a recent colonization of urban habitatMole. Ecol.12647656Google Scholar
  62. Weir, BS, Cockerham, CC 1984Estimating F statistics for the analysis of population structureEvolution3813581370Google Scholar
  63. White, PJ, Berry, WH, Eliason, JJ, Hanson, MT 2000Catastrophic decrease in an isolated population of kit foxesSouthwest. Nat.45204211Google Scholar
  64. White, PJ, Garrott, RA 1999Population dynamics of kit foxesCan. J. Zool.77486492Google Scholar
  65. White, PJ, Vanderbilt White, CA, Ralls, K 1996Functional and numerical responses of kit foxes to a short-term decline in mammalian preyJ. Mammal.77370376Google Scholar
  66. Whitlock, MC, McCauley, DE 1999Indirect measures of gene flow and migration: Fst≠ 1/(4Nm +1)Heredity82117125CrossRefPubMedGoogle Scholar
  67. Wright, S 1943Isolation by distanceGenetics28139156PubMedGoogle Scholar
  68. Wright, S 1969Evolution and the Genetics of Populations Volume 2: The theory of gene frequenciesUniversity of Chicago PressChicagoGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Michael K. Schwartz
    • 1
    • 2
  • Katherine Ralls
    • 3
  • Dan F. Williams
    • 4
  • Brian L. Cypher
    • 5
  • Kristine L. Pilgrim
    • 2
  • Robert C. Fleischer
    • 3
  1. 1.Wildlife Biology ProgramUniversity of MontanaMissoulaUSA
  2. 2.Rocky Mountain Research StationUSDA/USFSMissoula
  3. 3.Smithsonian InstitutionSmithsonian National Zoological ParkWashington
  4. 4.Department of Biological Sciences and Endangered Species Recovery ProgramCalifornia State UniversityStanislaus, Turlock
  5. 5.Endangered Species Recovery ProgramCalifornia State UniversityStanislaus, Bakersfield

Personalised recommendations