Skip to main content

Advertisement

SpringerLink
Log in

Dramatic shifts in the gene pool of a managed population of an endangered species may be exacerbated by high genetic load

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The Devils Hole pupfish, Cyprinodon diabolis, is restricted to a small habitat in southwestern Nevada. In 1972 the species was federally listed as an endangered species. Management efforts to mitigate extinction risks have been plagued by the inability to propagate the species in aquaria—anomalous for the genus—and repeated failure of propagation attempts in large, outdoor, artificial pools designed to mimic natural conditions in Devils Hole. These difficulties indicate that the species either has niche requirements that are not adequately recreated under artificial conditions or that it harbors a relatively large genetic load of deleterious mutations that compromises propagation. We used variation at 12 microsatellite loci to evaluate the results of natural, uncontrolled hybridization involving a population of C. diabolis inhabiting an artificial pool and invaders from a nearby population of the closely related C. nevadensis. The results suggest that following invasion of the pool by three C. nevadensis individuals, the gene pool underwent a rapid shift from pure C. diabolis to one comprised mostly of C. nevadensis alleles. Alleles diagnostic for C. nevadensis increased from about 0.03 to an average of 0.76 across four diagnostic loci over the course of 8 years or less. Although we cannot exclude explanations based on adaptation to Devils Hole, genetic drift, or demographic variability, these results and various other aspects of the biology of C. diabolis are best explained by the genetic load hypothesis. The work suggest avenues for future experimental work to evaluate these possibilities directly and provide an explanation for why some previous propagation efforts designed to mitigate extinction risk have failed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andersen ME, Deacon JE (2001) Population size of Devils Hole Pupfish (Cyprinodon diabolis) correlates with water level. Copeia 2001:224–228

    Article  Google Scholar 

  • Barrett PJ (2009) Estimating Devils Hole pupfish lifestage ratios using the Delphi Method. Fisheries 34:73–79

    Article  Google Scholar 

  • Barrett PJ, Deacon J (2009) Effects of climate change on Devils Hole and the Devils Hole pupfish, Cyprinodon diabolis. http://www.fws.gov/southwest/Climatechange/poster%20pdfs/DevilsHolePupfishPoster_BarrettandDeacon.pdf

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Ann Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Brown JH, Feldmeth CR (1971) Evolution in constant and fluctuating environments: thermal tolerances of desert Pupfish (Cyprinodon). Evolution 25:390–398

    Article  Google Scholar 

  • Burg TM, Wilcox JL, Martin A (2002) Isolation and characterization of polymorphic microsatellite loci in pupfish (genus Cyprinodon). Conserv Genet 3:197–204

    Article  CAS  Google Scholar 

  • Chernoff B (1985) Population dynamics of the Devils Hole pupfish. Environ Biol Fish 13:139–147

    Article  Google Scholar 

  • Cokendolpher JC (1980) Hybridization experiments with the genus Cyprinodon (Teleostei: Cyprinodontidae). Copeia 1980:173–176

    Article  Google Scholar 

  • Collyer ML, Novak JM, Stockwell CA (2005) Morphological divergence of native and recently established populations of White Sands Pupfish (Cyprinodon tularosa). Copeia 2005:1–11

    Article  Google Scholar 

  • Collyer ML, Stockwell CA, Adams DC, Reiser MH (2007) Phenotypic plasticity and contemporary evolution in introduced populations: evidence from translocated populations of White Sands Pupfish (Cyprinodon tularosa). Ecol Res 22:902–910

    Article  Google Scholar 

  • Deacon J, Deacon-Williams C (1991) Ash Meadows and the legacy of the Devils Hole Pupfish. In: Minckley WL, Deacon JE (eds) Battle against extinction: native fish management in the American West. University of Arizona Press, Tucson, pp 69–92

    Google Scholar 

  • Deacon JE, Taylor FR, Pedretti JW (1995) Egg viability and ecology of Devils Hole Pupfish: insights from captive propagation. Southwest Nat 40:216–223

    Google Scholar 

  • Duvernell DD, Turner BJ (1998) Evolutionary genetics of Death Valley pupfish populations: mitochondrial DNA sequence variation and population structure. Mol Ecol 7:279–288

    Article  Google Scholar 

  • Duvernell DD, Turner BJ (1999) Variation and divergence of Death Valley pupfish populations at retrotransposon-defined loci. Mol Biol Evol 16:363–371

    CAS  Google Scholar 

  • Echelle AA (2008) The western North American Pupfish clade (Cyprinodontidae: Cyprinodon): mitochondrial DNA divergence and drainage history. In: Reheis MC, Hershler R, Miller DM (eds) Late Cenozoic drainage history of the southwestern Great Basin and lower Colorado River region: geologic and biotic perspectives. Geological Society of America special paper 439, pp 27–38

  • Echelle AA, Connor PJ (1989) Rapid, geographically extensive genetic introgression after secondary contact between two Pupfish species (Cyprinodon, Cyprinodontidae). Evolution 43:717–727

    Article  Google Scholar 

  • Echelle AA, Dowling TE (1992) Mitochondrial DNA Variation and Evolution of the Death Valley Pupfishes (Cyprinodon, Cyprinodontidae). Evolution 46:193–206

    Article  CAS  Google Scholar 

  • Echelle AA, Echelle AF (1993) Allozyme perspective on mitochondrial DNA variation and evolution of the Death Valley Pupfishes (Cyprinodontidae: Cyprinodon). Copeia 1993:275–287

    Article  Google Scholar 

  • Eyre-Walker A, Keightley PD, Smith NGC, Gaffney D (2002) Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol 19:2142–2149

    Article  PubMed  CAS  Google Scholar 

  • Fisher MT (2000) Variation at major histocompatibility complex class I loci in two killifish species with reduced genetic variance. PhD dissertation, Virginia Polytechnic Institute and State University, Blacksburg

  • Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Hedrick P (2000) Genetics of populations, 2nd edn. Jones and Bartlett Publishing, Sudbury

    Google Scholar 

  • Hedrick P (2005) ‘Genetic restoration’: a more comprehensive perspective than ‘genetic rescue’. Trends Ecol Evol 20:109

    Article  PubMed  Google Scholar 

  • James CD (1969) Aspects of the ecology of Devils Hole Pupfish, Cyprinodon diabolis Wales. MS thesis, Nevada Southern University, Las Vegas

  • Johnson JE, Jensen BL (1991) Hatcheries for endangered freshwater fishes. In: Minckley WL, Deacon JE (eds) Battle against extinction: native fish management in the American West. University of Arizona Press, Tucson, pp 199–218

    Google Scholar 

  • Karam AP (2005) History and development of refuge management for Devils Hole pupfish (Cyprinodon diabolis) and an ecological comparison of three artificial refuges. MS Thesis, Southern Oregon University

  • Kinne O (1962) Irreversible non-genetic adaptation. Comp Biochem Physiol 5:265–282

    Article  PubMed  CAS  Google Scholar 

  • Lema SC (2006) Population divergence in plasticity of the AVT system and its association with aggressive behaviors in a Death Valley pupfish. Horm Behav 50:183–193

    Article  PubMed  CAS  Google Scholar 

  • Lema SC, Nevitt GA (2006) Testing an ecophysiological mechanism of morphological plasticity in Pupfish and its relevance to conservation efforts for endangered Devils Hole Pupfish. J Exp Biol 209:3499–3509

    Article  PubMed  Google Scholar 

  • Liu RK (1969) The comparative behavior of allopatric species (Teleostei-Cyprinodontidae: Cyprinodon). PhD dissertation, University of California, Los Angeles

  • Lynch M, Conery J, Burger R (1995) Mutational meltdown in sexual populations. Evolution 49:1067–1080

    Article  Google Scholar 

  • Martin AP (2005) Genetic analysis of Cyprinodon diabolis: hybridization With C. nevadensis in the Point of Rocks refuge. Nevada Division of Wildlife report

  • Martin AP (2010) The conservation genetics of Ash Meadows pupfish populations. I. The Warm Springs pupfish Cyprinodon nevadensis pectoralis. Conserv Gen 11:1847–1857

    Article  Google Scholar 

  • Martin AP, Wilcox JL (2004) Evolutionary history of Ash Meadows Pupfish (genus Cyprinodon) populations inferred using microsatellite markers. Conserv Gen 5:769–782

    Article  CAS  Google Scholar 

  • Miller RR (1981) Evolution of deserts and Pupfishes. In: Naiman RJ, Soltz DL (eds) Fishes in North American deserts. Wiley, New York, pp 383–404

    Google Scholar 

  • Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98

    Article  PubMed  CAS  Google Scholar 

  • Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Riggs AC, Deacon JE (2002) Connectivity in desert aquatic ecosystems: The Devils Hole story. In: Sada DW, Sharpe SE (eds) Spring-fed wetlands: important scientific and cultural resources of the intermountain region conference proceedings. http://www.wetlands.dri.edu/2002/Riggs-Deacon.pdf, November 2007

  • Rosenfield JA, Kodric-Brown A (2003) Sexual selection promotes hybridization between Pecos pupfish, Cyprinodon pecosensis and sheepshead minnow, C. variegatus. J Evol Biol 16:595–606

    Article  PubMed  CAS  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Rowe G, Beebee TJC (2003) Population on the verge of a mutational meltdown? Fitness costs of genetic load for an amphibian in the wild. Evolution 57:177–181

    PubMed  Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Mol Ecol 82:561–573

    Google Scholar 

  • Soltz DL, Naiman RJ (1978) The natural history of native fishes in the Death Valley System. Nat Hist Mus Los Angel Cty Calif Sci Ser 30:1–76

    Google Scholar 

  • Sutherlands GR, Richards RI (1995) Simple tandem DNA repeats and human disease. Proc Natl Acad Sci USA 92:3636–3641

    Article  Google Scholar 

  • Sweet JG, Kinne O (1964) The effects of various temperature-salinity combinations on the body form of newly hatched Cyprinodon macularius (Teleostei). Helgolaender Wissenschaftliche Meeresunter-suchungen 11:49–69

    Article  Google Scholar 

  • Turner BJ (1974) Genetic divergence of Death Valley pupfish species: biochemical versus morphological evidence. Evolution 28:281–294

    Article  Google Scholar 

  • USFWS, US Fish and Wildlife Service (2009) Spotlight species action plan 2010-2014. http://ecos.fws.gov/docs/action_plans/doc3170.pdf

  • Wilcox JL, Martin AP (2006) The devil’s in the details: genetic and phenotypic divergence between artificial and native populations of the endangered pupfish (Cyprinodon diabolis). Anim Conserv 9:316–321

    Article  Google Scholar 

  • Wilson KP, Blinn DW (2007) Food web structure, energetics, and importance of allochthonous carbon in a desert cavernous limnocrene: Devils Hole, Nevada. West North Am Nat 67:185–198

    Article  Google Scholar 

Download references

Acknowledgments

Many individuals provided assistance, samples and funding to complete this project. Cynthia Martinez, Nevada Ecological Services Field Office of the United States Fish and Wildlife Service (USFWS) secured funding through the Directors’ Priority Projects and Manuel Ulibarri, Dexter National Fish Hatchery and Technology Center (USFWS) provided project oversight. Bruce Turner provided some tissue samples and Wade Wilson and Teresa Lewis provided internal reviews. Others that have contributed time and effort to this project include Cristi Baldino, Sharon McKelvey, Shawn Goodchild, Darrick Weissenfluh, Jim Heinrich, Brian Hobbs, and Jennifer Wilcox. The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the U.S. Fish and Wildlife Service.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309, USA

    Andrew P. Martin

  2. Zoology Department, Oklahoma State University, Stillwater, OK, 74078, USA

    Anthony A. Echelle

  3. Department of Biology, University of Maine, Machias, ME, 04654, USA

    Gerard Zegers

  4. Molecular Ecology Program, Dexter NFHTC, P.O. Box 219, Dexter, NM, 88230, USA

    Sherri Baker & Connie L. Keeler-Foster

Authors
  1. Andrew P. Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony A. Echelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gerard Zegers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sherri Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Connie L. Keeler-Foster
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrew P. Martin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martin, A.P., Echelle, A.A., Zegers, G. et al. Dramatic shifts in the gene pool of a managed population of an endangered species may be exacerbated by high genetic load. Conserv Genet 13, 349–358 (2012). https://doi.org/10.1007/s10592-011-0289-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-011-0289-7

Keywords

Search

Navigation