Skip to main content

Advertisement

Log in

High and dry: intermittent watersheds provide a test case for genetic response of desert fishes to climate change

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

Abstract

In desert streams, fishes and other organisms that depend on surface water are predicted to inhabit smaller and more isolated wetted reaches, while the frequency and severity of disturbance is expected to increase under most climate change models. Together, these factors should reduce population genetic diversity and persistence probabilities. In this study, our goal was to understand genetic responses of stream fish populations to disturbance in an intermittent stream network. This network is occupied by Rio Grande sucker (Pantosteus plebeius) that is native to highland desert streams in North America. Sample localities in upland perennial reaches were connected by moderate to high levels of gene flow even when separated by up to a 30-km intermittent reach. However, drier and lower-elevation reaches were significant barriers to gene flow. Effects of genetic drift (lower allelic diversity and higher levels of inbreeding) were more pronounced in the watershed with fewest wetted reaches. Temporal analysis of genetic diversity indicated that streams with several spatially distinct wetted reaches were more genetically resistant to wildfire-induced demographic bottlenecks than a stream with only one wetted reach. Maintenance of multiple wetted reaches within streams and facilitated gene flow among watersheds could slow losses of genetic diversity in upland desert stream fishes, and will be important strategies for conserving stream biodiversity in the face of habitat fragmentation and disturbance related to climate change.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allan JD, Flecker AS (1993) Biodiversity conservation in running waters. Bioscience 43:32–43

    Article  Google Scholar 

  • Brown JH (1971) Mammals on mountaintops: nonequilibrium insular biogeography. Am Nat 105:467–478

    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 

  • Calamusso B, Rinne JR, Turner PR (2002) Distribution and abundance of the Rio Grande sucker in the Carson and Santa Fe National forests, New Mexico. Southwest Nat, 47:182–186

  • Clarkson RW, Marsh PC, Dowling TE (2012) Population prioritization for conservation of imperiled warmwater fishes in an arid-region drainage. Aquat Conserv Mar Freshw Ecosyst 22:498–510

    Article  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Dunham JB, Young MK, Gresswell RE, Rieman BE (2003) Effects of fire on fish populations: landscape perspectives on persistence of native fishes and nonnative fish invasions. For Ecol Manag 178:183–196

    Article  Google Scholar 

  • Earl DA, Von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Echelle AA, Carson EW, Echelle AF, Van Den Bussche RA, Dowling TE, Meyer A (2005) Historical biogeography of the new-world pupfish genus Cyprinodon (Teleostei: Cyprinodontidae). Copeia 2005:320–339

    Article  Google Scholar 

  • 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

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed Central  CAS  Google Scholar 

  • 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 19:4723–4737

    Article  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

    Article  PubMed  Google Scholar 

  • Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinctions. In: Soulé ME (ed) Conservation biology–the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 19–34

    Google Scholar 

  • Gomez-Uchida D, Palstra FP, Knight TW, Ruzzante DE (2013) Contemporary effective population and metapopulation size (N e and meta-N e ): comparison among three salmonids inhabiting a fragmented system and differing in gene flow and its asymmetries. Ecol Evol 3:569–580

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Gutzler DS (2013) Regional climatic considerations for borderlands sustainability. Ecosphere. doi:10.1890/ES12-00283.1

    Google Scholar 

  • Heald WF (1967) Sky island. Van Nostren, Princeton

    Google Scholar 

  • Higgins K, Lynch M (2001) Metapopulation extinction caused by mutation accumulation. Proc Natl Acad Sci USA 98:2928–2933

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  • Hillis D, Moritz C, Mable B (1996) Molecular systematics. Sinauer, Sunderland

    Google Scholar 

  • Hoagstrom CW, Brooks JE, Davenport SR (2011) A large-scale conservation perspective considering endemic fishes of the North American plains. Biol Conserv 144:21–34

    Article  Google Scholar 

  • Hurd BH, Coonrod J (2007) Climate change and its implications for New Mexico’s water resources and economic opportunities. National Commission on Energy Policy. New Mexico State University, Las Cruces

    Google Scholar 

  • Hutchison DW, Templeton AR (1999) Correlation of pairwise genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution 53:1898–1914

    Article  Google Scholar 

  • Isaak DJ, Luce CH, Rieman BE, Nagel DE, Peterson EE, Horan DL, Parkes S, Chandler GL (2010) Effects of climate change and wildfire on stream temperatures and salmonid thermal habitat in a mountain river network. Ecol Appl 20:1350–1371

    Article  PubMed  Google Scholar 

  • Jaeger KL, Olden JD, Pelland ND (2014) Climate change poised to threaten hydrologic connectivity and endemic fishes in dryland streams. Proc Natl Acad Sci USA. doi:10.1073/pnas.1320890111

    PubMed Central  Google Scholar 

  • Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935

    Article  PubMed Central  PubMed  Google Scholar 

  • Kalinowski ST, Meeuwig MH, Narum SR, Taper ML (2008) Stream trees: a statistical method for mapping genetic differences between populations of freshwater organisms to the sections of streams that connect them. Can J Fish Aquat Sci 65:2752–2760

    Article  Google Scholar 

  • Kennedy TL, Gutzler DS, Leung RL (2009) Predicting future threats to the long-term survival of Gila trout using a high-resolution simulation of climate change. Clim Change 94:503–515

    Article  Google Scholar 

  • Kodric-Brown A, Brown JH (1993) Highly structured fish communities in Australian desert springs. Ecology 74:1847–1855

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477–494

    Article  Google Scholar 

  • Lyon JP, O’Connor JP (2008) Smoke on the water: can riverine fish populations recover following a catastrophic fire-related sediment slug? Austral Ecol 33:794–806

    Article  Google Scholar 

  • McPhee MV (2007) Age, growth and life history comparisons between the invasive white sucker (Catostomus commersoni) and native Rio Grande sucker (C. plebeius). Southwest Nat 52:15–25

    Article  Google Scholar 

  • McPhee MV, Osborne MJ, Turner TF (2008) Genetic diversity, population structure, and demographic history of the Rio Grande Sucker, Catostomus (Pantosteus) plebeius, in New Mexico. Copeia 2008:191–199

    Article  Google Scholar 

  • Miller RR, Minckley WL, Norris SM (2005) Freshwater fishes of Mexico. University of Chicago Press, Chicago

    Google Scholar 

  • Minckley WL, Marsh PC (2009) Inland fishes of the greater Southwest: chronicle of a vanishing biota. University of Arizona Press, Tucson

    Google Scholar 

  • Neel MC, McKelvey K, Ryman N, Lloyd MW, Short Bull R, Allendorf FW, Schwartz MK, Waples RS (2013) Estimation of effective population size in continuously distributed populations: there goes the neighborhood. Heredity 111:189–199

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nunney L (1999) The effective size of a hierarchically structured population. Evolution 53:1–10

    Article  Google Scholar 

  • Petit RJ, El Mousadik A, Pons P (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rinne JN (1995) Reproductive biology of the Rio Grande sucker Catostomus plebeius (Cypiniformes), in a montane stream, New Mexico. Southwest Nat 40:237–241

    Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetics data analysis. Ver 2.000. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva

  • Seager R, Ting M, Held I, Kushnir Y, Lu J et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1183

    Article  CAS  PubMed  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Sublette EJ, Hatch DM, Sublette M (1990) The fishes of New Mexico. University of New Mexico Press, Albuquerque

    Google Scholar 

  • Swift-Miller SM, Johnson BM, Muth RT, Langlois D (1999) Distribution, abundance, and habitat use of Rio Grande sucker (Catostomus plebeius) in Hot Creek, Colorado. Southwest Nat 44:42–48

    Google Scholar 

  • Tranah GJ, Agresti JJ, May B (2001) New microsatellite loci for suckers (Catostomidae): primer homology in Catostomus, Chasmistes, and Deltistes. Mol Ecol Notes 1:55–60

    Article  CAS  Google Scholar 

  • Turner TF, Osborne MJ, Dowling TE, McPhee MV, Broughton RE, Gold JR (2009) Microsatellite markers for the endangered razorback sucker, Xyrauchen texanus, are widely applicable to genetic studies of other catostomine fishes. Conser Genet 10:551–553

    Article  CAS  Google Scholar 

  • Unmack PJ, Dowling TE, Laitinen NJ, Secor CL, Mayden RL, Shiozawa DK, Smith GR (2014) Influence of introgression and geological processes on phylogenetic relationships of western North American mountain suckers. (Pantosteus, Catostomidae). PLoS One 9:e90061. doi:10.1371/journal.pone.0090061

    Article  PubMed Central  PubMed  Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352

    Article  CAS  PubMed  Google Scholar 

  • Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed Central  PubMed  Google Scholar 

  • Westerling AL, Hidalgo HG, Cayan DR, Swetnam TW (2006) Warming and earlier spring increase western U.S. forest wildfire activity. Science 313:940–943

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Heather Johnson, Eric Leinonen, and Michael Konsmo for field assistance. Krista Leibensperger, Tyler Pilger, Hailey Conover, and George Rosenberg provided assistance in the laboratory. Genotyping was done in the UNM Molecular Biology Facility supported, in part, by NIH grant number P20GM103452. David Propst, Tyler Pilger, John Carlos Garza, and an anonymous reviewer made valuable comments and suggestions that greatly improved the manuscript. Field collections were made under New Mexico Department of Game and Fish Authorization for Taking Protected Wildlife For Scientific and Educational Purposes Permit # 3261 and UNM IACUC Protocol # 10-100492-MCC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas F. Turner.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 13 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turner, T.F., Osborne, M.J., McPhee, M.V. et al. High and dry: intermittent watersheds provide a test case for genetic response of desert fishes to climate change. Conserv Genet 16, 399–410 (2015). https://doi.org/10.1007/s10592-014-0666-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0666-0

Keywords

Navigation