Conservation Genetics

, Volume 16, Issue 3, pp 743–758 | Cite as

Conservation genetics of a desert fish species: the Lahontan tui chub (Siphateles bicolor ssp.)

  • Amanda J. Finger
  • Bernie May
Research Article


Analysis of the genetic diversity and structure of declining populations is critical as species and populations are increasingly fragmented globally. In the Great Basin Desert in particular, climate change, habitat alteration, and fragmentation threaten aquatic habitats and their endemic species. Tui chubs, including the Lahontan tui chub and Dixie Valley tui chub, (Siphateles bicolor ssp.) are native to the Walker, Carson, Truckee and Humboldt River drainages in the Great Basin Desert. Two populations, Walker Lake and Dixie Valley, are under threat from habitat alteration, increased salinity, small population sizes, and nonnative species. We used nine microsatellite markers to investigate the population genetic structure and diversity of these and nine other tui chub populations to provide information to managers for the conservation of both Walker Lake and Dixie Valley tui chubs. Genetic population structure reflects both historical and contemporary factors, such as connection with Pleistocene Lake Lahontan in addition to more recent habitat fragmentation. Dixie Valley was the most highly differentiated population (pairwise F ST = 0.098−0.217, p < 0.001), showed evidence of a past bottleneck, and had the lowest observed heterozygosity (Ho = 0.607). Walker Lake was not substantially differentiated from other Lahontan tui chub populations, including those located in different watersheds (pairwise F ST = 0.031−0.103, p < 0.001), and had the highest overall observed heterozygosity (Ho = 0.833). We recommend that managers continue to manage and monitor Dixie Valley as a distinct Management Unit, while continuing to maximize habitat size and quality to preserve overall genetic diversity, evolutionary potential, and ecological processes.


Microsatellite Desert fishes Tui chub Great Basin Walker Lake Dixie Valley 



The authors would like to thank Kathleen Fisch, Mariah Meek, Ben Sacks, Karrigan Bork, Molly Stephens, and three anonymous reviewers for valuable comments. We would also like to thank NDOW biologists Kim Tisdale, Karie Wright, and Kris Urqhart for samples, insight, and a greater understanding of tui chub populations. Funding for this project was provided by Nevada Department of Wildlife, Task order 84240-9-J002; CESU agreement 81332-5-G004.


  1. Avise JC (2000) Phylogeography. The history and formation of species. Harvard University Press, Cambridge, MAGoogle Scholar
  2. Baerwald MR, May B (2004) Characterization of microsatellite loci for five members of the minnow family Cyprinidae found in the Sacramento-San Joaquin Delta and its tributaries. Mol Ecol Notes 4:385–390CrossRefGoogle Scholar
  3. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2003) GENETIX version 4.04, logiciel sous WindowsTM pour la genetique des populations. Laboratoire Genome, Populations, Interactions: CNRS UMR. 5000, Universite de Montpellier II, Montpellier, FranceGoogle Scholar
  4. Benson LV (1991) Timing of the last highstand of Lake Lahontan. J Paleolimnol 5:115–126CrossRefGoogle Scholar
  5. Caughley G (1994) Directions in conservation biology. J Anim Ecol 63(2):215–244CrossRefGoogle Scholar
  6. Chen YZ (2013) Genetic characterization and management of the endangered Mohave tui chub. Conserv Genet 14:11–20CrossRefGoogle Scholar
  7. Coffin PD, Cowan WF (1995) Lahontan cutthroat trout (Oncorhynchus clarki henshawi) recovery plan. U. S. Fish and Wildlife Service, PortlandGoogle Scholar
  8. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedCentralPubMedGoogle Scholar
  9. Di Rienzo A, Peterson A, Garza J, Valdes A, Slatkin M, Freimer N (1994) Mutational processes of simple-sequence repeat loci in human populations. PNAS 91:3166–3170CrossRefPubMedCentralPubMedGoogle Scholar
  10. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovendon JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective size (N e) from genetic data. Mol Ecol Resour 14:209–214CrossRefPubMedGoogle Scholar
  11. Dowling T, Minckley W, Marsh P (1996a) Mitochondrial DNA diversity within and among populations of razorback sucker (Xyrauchen taxanus) as determined by restriction endonuclease analysis. Copeia 1996:542–550CrossRefGoogle Scholar
  12. Dowling T, Minckley W, Marsh P, Goldstein E (1996b) Mitochondrial DNA diversity in the endangered razorback sucker (Xyrauchen texanus): analysis of hatchery stocks and implications for captive propagation. Conserv Biol 10:120–127CrossRefGoogle Scholar
  13. Dowling T, Marsh P, Kelsen A, Tibbets C (2005) Genetic monitoring of wild and repatriated populations of endangered razorback sucker (Xyrauchen texanus, Catostomidae, Teleostei) in Lake Mohave, Arizona-Nevada. Mol Ecol 14:123–136CrossRefPubMedGoogle Scholar
  14. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  15. Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In: Carvlho GR (ed) Advances in molecular ecology. NATO Science Series, IOS Press, Amsterdam, pp 55–86Google Scholar
  16. Estoup A, Cornuet JM (1999) Microsatellite evolution: inferences from population data. In: Goldstein DB, Schlöterrer C (eds) Microsatellites: evolution and applications. Oxford University Press, Oxford, pp 49–65Google Scholar
  17. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  18. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetic analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  19. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotyped data: linked loci and correlated allele frequences. Genetics 164(4):1567–1587Google Scholar
  20. Faulks LK, Gilligan DM, Beheregaray LB (2010) Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia’s arid zone, the golden perch (Macquaria ambigua). Mol Ecol 19:4723–4737CrossRefPubMedGoogle Scholar
  21. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  22. Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–73CrossRefGoogle Scholar
  23. Garrigan D, Marsh PC, Dowling TE (2002) Long-term effective population size of three endangered Colorado Fishes. Anim Conserv 5:95–102CrossRefGoogle Scholar
  24. Garside LJ, Schilling JH (1979) Thermal waters of Nevada: Nevada bureau of mines and geology. Bulletin 91:163Google Scholar
  25. Garza JK, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10(2):305–318Google Scholar
  26. Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer and Associates, Sunderland, pp 19–34Google Scholar
  27. Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS One 7(9):e45170CrossRefPubMedCentralPubMedGoogle Scholar
  28. Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  29. Hardy OJ, Charbonnel N, Freville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482PubMedCentralPubMedGoogle Scholar
  30. Harris PM (2000) Systematic studies of the genus Siphateles (Ostariophysi: Cyprinidae) from western North America. PhD dissertation, Oregon State UniversityGoogle Scholar
  31. Hedrick PC (2004) Recent developments in conservation genetics. Forest Ecol Manag 197:3–19CrossRefGoogle Scholar
  32. Hernandez-Martich JD, Smith MA (1997) Downstream gene flow and genetic structure of Gambusia holbrooki (eastern mosquitofish). Heredity 79:295–301CrossRefGoogle Scholar
  33. Hershler R (1998) A systematic review of hydrobiid snails (Gastropoda: Risooidea) of the Great Basin, Western United States, Part I: Genus Pyrgulopsis. Veliger 41:1–132Google Scholar
  34. Hubbs CL, Miller RR (1948) The zoological evidence: correlation between fish distribution and hydrographic history in the desert basins of Western United States. In: The Great Basin, with emphasis on glacial and postglacial times. Bulletin of the University of Utah, vol 38. pp 17–166Google Scholar
  35. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  36. Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584CrossRefPubMedGoogle Scholar
  37. Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543CrossRefGoogle Scholar
  38. Kalinowski ST (2005a) Do polymorphic loci require large sample sizes to estimate genetic distances? Heredity 94:33–36CrossRefPubMedGoogle Scholar
  39. Kalinowski ST (2005b) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189CrossRefGoogle Scholar
  40. Kimsey JB (1954) The life history of the tui chub Siphateles bicolor (Girard) from Eagle Lake, California. Calif Fish Game 40:395–410Google Scholar
  41. Kucera PA (1978) Reproductive biology of the tui chub, Gila bicolor, in Pyramid Lake, Nevada. Great Basin Nat 38(2):203–207Google Scholar
  42. Kuo C, Janzen F (2004) Genetic effects of a persistent bottleneck on a natural population of ornate box turtles (Terrapene ornata). Conserv Genet 5:425–437CrossRefGoogle Scholar
  43. Lande R (1993) Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am Nat 142(6):911–927CrossRefGoogle Scholar
  44. Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data. Version 1.0 (d16c) Free program distributed by the authors over the internet from
  45. Lippe C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae: Pisces): the positive sides of long generation time. Mol Ecol 15:1769–1780CrossRefPubMedGoogle Scholar
  46. Lopes TJ, Allender KK (2009) Water budgets of the Walker River basin and Walker Lake, California and Nevada: U.S. Geological Survey Scientific Investigations. Report 2009–5157:44pGoogle Scholar
  47. Lynch M, Lande R (1998) The critical effective size for a genetically secure population. Anim Conserv 1:70–72CrossRefGoogle Scholar
  48. May B (1999) Genetic purity and subspecific status of the Dixie Valley tui chub. Report to the Department of the Navy, N68711-98-LT-80018Google Scholar
  49. Meredith EP, May B (2002) Microsatellite loci in the Lahontan tui chub, Gila bicolor obesa, and their utilization in other chub species. Mol Ecol Notes 2:156–158CrossRefGoogle Scholar
  50. Moritz C (1994) Defining ‘Evolutionarily significant units’ for conservation. Trends Ecol Evol 9(10):373–375CrossRefPubMedGoogle Scholar
  51. Moyle PB, Yoshiyama RM, Williams JE, Wikramanayake ED (1995) Fish species of special concern in California. Final Report for Contract N. 2128IF to California Department of Fish and GameGoogle Scholar
  52. Nevada Department of Wildlife (2011) Walker Lake Fishery Improvement Program. Final Report for FWS Cooperative Agreement No. 84240-6-J, 52 ppGoogle Scholar
  53. Nomura T (2008) Estimation of effective number of breeders from molecular ancestry of single cohort sample. Evol Appl 1(3):462–474Google Scholar
  54. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vasquez-Carillo C, Pauli JN, Palsboll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418CrossRefPubMedGoogle Scholar
  55. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. Heredity 90:502–503CrossRefGoogle Scholar
  56. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  57. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  58. Raymond AW, Sobel E (1990) The use of tui chub as food by Indians of the Western Great Basin. J Cailf Great Basin Anthropol 12:2–18Google Scholar
  59. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43(1):223–225Google Scholar
  60. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  61. Russell IC (1885) Geological History of Lake Lahontan, A Quaternary Lake of Northwestern Nevada. Monograph XI, Geological Survey, U.S. Department of the Interior, Government Printing Office, Washington, D. CGoogle Scholar
  62. Sada DW, Vineyard GL (2002) Anthropogenic changes in biogeography of Great Basin Aquatic Biota. Smithson Contrib Earth Sci 33:277–293Google Scholar
  63. Scoppettone GG, Coleman M, Wedemeyer GA (1986) Life history and status of the endangered cui-ui of Pyramid Lake, Nevada. U.S Fish and wildlife service. Fish Wildl Res 1:1–23Google Scholar
  64. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. TREE 22(1):25–33Google Scholar
  65. Smith GR, Dowling TE, Gobalet KW, Lugaski T, Shiazawa D, Evans RP (2002) Biogeography and timing of evolutionary events amont Great Basin fishes. In: R Hershler, DB Madsen, Curry DR (eds) Great Basin aquatic systems history, smithsonian contributions to earth sciences, vol 33. pp 175–234Google Scholar
  66. Spencer CC, Neigel JE, Leberg PL (2000) Experimental evaluation of the usefulness of microsatellite DNA for detecting demographic bottlenecks. Mol Ecol 9:1517–1528CrossRefPubMedGoogle Scholar
  67. Stockwell CA (1994) The biology of Walker Lake, The University Report. Department of Biology, University of Nevada, RenoGoogle Scholar
  68. U.S. Fish and Wildlife Service (1985) Endangered and threatened wildlife and plants: review of vertebrate wildlife; Notice of review. Federal Register 50 CFR Part 17Google Scholar
  69. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotype errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  70. Waples RS, C Do (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756Google Scholar
  71. Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3(3):244–262CrossRefPubMedCentralPubMedGoogle Scholar
  72. Zhdanova OL, Pudovkin AI (2008) Nb_HetEx: a program to estimate the effective number of breeders. J Hered 99(6):694–695Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Genomic Variation Lab, Department of Animal ScienceUniversity of California, DavisDavisUSA

Personalised recommendations