Skip to main content

Advertisement

Log in

Water availability strongly impacts population genetic patterns of an imperiled Great Plains endemic fish

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

Abstract

Genetic, demographic, and environmental processes affect natural populations synergistically, and understanding their interplay is crucial for the conservation of biodiversity. Stream fishes in metapopulations are particularly sensitive to habitat fragmentation because persistence depends on dispersal and colonization of new habitat but dispersal is constrained to stream networks. Great Plains streams are increasingly fragmented by water diversion and climate change, threatening connectivity of fish populations in this ecosystem. We used seven microsatellite loci to describe population and landscape genetic patterns across 614 individuals from 12 remaining populations of Arkansas darter (Etheostoma cragini) in Colorado, a candidate species for listing under the U.S. Endangered Species Act. We found small effective population sizes, low levels of genetic diversity within populations, and high levels of genetic structure, especially among basins. Both at- and between-site landscape features were associated with genetic diversity and connectivity, respectively. Available stream habitat and amount of continuous wetted area were positively associated with genetic diversity within a site, while stream distance and intermittency were the best predictors of genetic divergence among sites. We found little genetic contribution from historic supplementation efforts, and we provide a set of management recommendations for this species that incorporate a conservation genetics perspective.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5

Similar content being viewed by others

References

  • Amos W, Wilmer JW, Fullard K et al (2001) The influence of parental relatedness on reproductive success. Proc R Soc B Biol Sci 268:2021–2027

    Article  CAS  Google Scholar 

  • Araki H, Cooper B, Blouin M (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103

    Article  CAS  PubMed  Google Scholar 

  • Araki H, Berejikian B, Ford M, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355

    Article  PubMed Central  Google Scholar 

  • Araki H, Cooper B, Blouin MS (2009) Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild. Biol Lett 5:621–624

    Article  PubMed Central  PubMed  Google Scholar 

  • Austin JD, Jelks HL, Tate B, Johnson AR, Jordan F (2011) Population genetic structure and conservation genetics of threatened Okaloosa darters (Etheostoma okaloosae). Conserv Genet 12:981–989

    Article  Google Scholar 

  • Benda L, Poff NL, Miller D, Dunne T, Reeves G, Pess G, Pollock M (2004) The network dynamics hypothesis: how channel networks structure riverine habitats. Bioscience 54:413–427

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Ecol Modell 172:488

    Google Scholar 

  • Campbell-Grant EH, Lowe WH, Fagan WF (2007) Living in the branches: population dynamics and ecological processes in dendritic networks. Ecol Lett 10:165–175

    Article  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Christie MR, Marine ML, French RA, Blouin MS (2011) Genetic adaptation to captivity can occur in a single generation. Proc Natl Acad Sci 109:238–242

    Article  PubMed Central  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cosentino BJ, Phillips CA, Schooley RL et al (2011) Linking extinction–colonization dynamics to genetic structure in a salamander metapopulation. Proc Biol Sci 279:1575–1582

    Article  PubMed Central  PubMed  Google Scholar 

  • Davis MB, Shaw RG (2001) Range shifts and adaptive responses to quaternary climate change. Science 292:673–679

    Article  CAS  PubMed  Google Scholar 

  • Dodds WK, Gido K, Whiles MR et al (2004) Life on the edge: the ecology of Great Plains prairie streams. Bioscience 54:205–216

    Article  Google Scholar 

  • Eberle ME, Stark WJ (2000) Status of the Arkansas darter in south-central Kansas and adjacent Oklahoma. Prairie Nat 32:103–113

    Google Scholar 

  • Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475

    Article  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:147–150

    Google Scholar 

  • Fagan WF (2002) Connectivity, fragmentation, and extinction risk in dendritic metapopulations. Ecology 83:3243–3249

    Article  Google Scholar 

  • Fagan WF, Holmes EE (2006) Quantifying the extinction vortex. Ecol Lett 9:51–60

    PubMed  Google Scholar 

  • Fagan WF, Unmack P, Burgess C, Minckley WL (2002) Rarity, fragmentation, and extinction risk in desert fishes. Ecology 83:3250–3256

    Article  Google Scholar 

  • Falke J, Fausch K (2010) From metapopulations to metacommunities: linking theory with empirical observations of the spatial population dynamics of stream fishes. In: Gido K, Jackson D (eds), Community ecology of stream fishes: concepts, approaches, and techniques. American Fisheries Society, Symposium 73, Bethesda, pp 207–233

  • Falke JA, Fausch KD, Magelky R et al (2011) The role of groundwater pumping and drought in shaping ecological futures for stream fishes in a dryland river basin of the western Great Plains, USA. Ecohydrology 697:682–697

    Article  Google Scholar 

  • Fausch KD, Bestgen KR (1997) Ecology of fishes indigenous to the central and southwestern Great Plains. In: Knopf FL, Samson FB (eds) Ecology and conservation of Great Plains vertebrates. Springer, Verlag, pp 131–166

    Chapter  Google Scholar 

  • Feminella JW, Matthews WJ (1984) Intraspecific differences in thermal tolerances of Etheostoma spectabile in constant versus fluctuating environments. J Fish Bio 25:455–461

    Article  Google Scholar 

  • Fleming L, Gross M (1994) Breeding competition in a Pacific salmon (coho, Oncorhyncus kisutch)—measures of natural and sexual selection. Evolution 48:637–657

    Article  Google Scholar 

  • Fluker BL, Kuhajda BR, Lang NJ, Harris PM (2010) Low genetic diversity and small long-term population sizes in the spring endemic watercress darter, Etheostoma nuchale. Conserv Genet 11:2267–2279

    Article  Google Scholar 

  • Frankham R (1995a) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:491–503

    Article  Google Scholar 

  • Frankham R (1995b) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–799

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed  Google Scholar 

  • Gaggiotti OE, Hanski I (2004) Mechanisms of population extinction. In: Hanski IA, Gaggiotti OE (eds) Ecology genetics and evolution of metapopulations. Elsevier Academic Press, Philadelphia, pp 337–366

    Chapter  Google Scholar 

  • George AL, Kuhajda BR, Williams JD, Cantrell MA, Rakes PL, Shute JR (2009) Guidelines for propagation and translocation for freshwater fish conservation. Fisheries 34:529–545

    Article  Google Scholar 

  • Goslee S (2010) Correlation analysis of dissimilarity analysis. Plant Ecol 206:279–286

    Article  Google Scholar 

  • Goslee S, Urban D (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Google Scholar 

  • Graham MH (2003) Confronting multicollinearity in ecological multiple regression. Ecology 84:2809–2815

    Article  Google Scholar 

  • Groce MC, Bailey LL, Fausch KD (2012) Evaluating the success of Arkansas darter translocations in Colorado: an occupancy sampling approach. Trans Am Fish Soc 141:825–840

    Article  Google Scholar 

  • Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Gutentag E, Heimes F, Krothe N et al (1984) Geohydrology of the High Plains Aquifer in parts of Colorado, Kansas, Nebraska, New Mexico, Oklahoma, South Dakota, Texas, and Wyoming. USGS Professional Paper 1400-B

  • Hansen MM, Fraser DJ, Meier K, Mensberg KD (2009) Sixty years of anthropogenic pressure: a spatio-temporal genetic analysis of brown trout populations subject to stocking and population declines. Mol Ecol 18:2549–2562

    Article  CAS  PubMed  Google Scholar 

  • Hanski I (1998) Metapopulation dynamics. Nature 396:41–49

    Article  CAS  Google Scholar 

  • Hanski I, Gilpin M (1997) Metapopulation biology: ecology, genetics, and evolution. Academic Press, New York

    Google Scholar 

  • Hargrave CW, Johnson JE (2003) Status of Arkansas darter, Etheostoma cragini, and least darter, E. microperca, in Arkasas. Southwest Nat 48:89–92

    Article  Google Scholar 

  • Harrison S (1991) Local extinction in a metapopulation context: an empirical evaluation. Biol J Linn Soc 42:73–88

    Article  Google Scholar 

  • Helfman GS (2007) Fish conservation: a guide to understanding and restoring global aquatic biodiversity and fishery resources. Island Press, Washington, D.C.

    Google Scholar 

  • Hudman S, Grose M, Landis J et al (2008) Twenty-three microsatellite DNA loci for population genetic studies and parentage assignment in orangethroat darter, Etheostoma spectabile. Mol Ecol Resour 8:1483–1485

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2005) HP-Rare: a computer program for performing rarefaction on measures of allelic diversity. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Kanno Y, Vokoun JC, Letcher BH (2011) Fine-scale population structure and riverscape genetics of brook trout (Salvelinus fontinalis) distributed continuously along headwater channel networks. Mol Ecol 20:3711–3729

    Article  PubMed  Google Scholar 

  • Koskinen MT, Sundell P, Piironen J, Primmer CR (2002) Genetic assessment of spatiotemporal evolutionary relationships and stocking effects in grayling (Thymallus thymallus, Salmonidae). Ecol Lett 5:193–205

    Article  Google Scholar 

  • Krieger D, Nesler T, Bennet C et al (2001) Arkansas darter (Etheostoma cragini) recovery plan. Denver

  • Kuehne RA, Barbour RW (1983) The American darters. University of Kentucky Press, Lexington

    Google Scholar 

  • Labbe TR, Fausch KD (2000) Dynamics of intermittent stream habitat regulate persistence of a threatened fish at multiple scales. Ecol Appl 10:1774–1791

    Article  Google Scholar 

  • Labonne J, Ravigne V, Parisi B (2008) Linking dendritic network structures to population demogenetics: the downside of connectivity. Oikos 117:1479–1490

    Article  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241(80):1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  • Letcher BH, Nislow KH, Coombs JA et al (2007) Population response to habitat fragmentation in a stream-dwelling brook trout population. Public Libr Sci. doi:10.1371/journal.pone.0001139

    Google Scholar 

  • Lichstein J (2007) Multiple regression on distance matrices: a multivariate spatial analysis tool. Plant Ecol 188:117–131

    Article  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA et al (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    Article  CAS  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Marie AD, Bernatchez L, Garant D (2010) Loss of genetic integrity correlates with stocking intensity in brook charr (Salvelinus fontinalis). Mol Ecol 19:2025–2037

    Article  CAS  PubMed  Google Scholar 

  • McCusker MR, Bentzen P (2010) Positive relationships between genetic diversity and abundance in fishes. Mol Ecol 19:4852–4862

    Article  PubMed  Google Scholar 

  • Meeuwig MH, Guy CS, Kalinowski ST, Fredenberg WA (2010) Landscape influences on genetic differentiation among bull trout populations in a stream-lake network. Mol Ecol 19:3620–3633

    Article  PubMed  Google Scholar 

  • Miller DL (1984) Distribution, abundance, and habitat of the Arkansas darter Etheostoma cragini (Percidae) in Colorado. Southwest Nat 29:496–499

    Article  Google Scholar 

  • Mills LS, Smouse PE (1994) Demographic consequences of inbreeding in remnant populations. Am Nat 144:412–431

    Article  Google Scholar 

  • Milly PCD, Dunne KA, Vecchia AV (2005) Global pattern of trends in streamflow and water availability in a changing climate. Nature 438:347–350

    Article  CAS  PubMed  Google Scholar 

  • Murphy M, Dezzani R, Pilliod D, Storfer A (2010) Landscape genetics of high mountain frog metapopulations. Mol Ecol 19:3634–3649

    Article  PubMed  Google Scholar 

  • Naish KA, Taylor JE, Levin PS et al (2007) An evaluation of the effects of conservation and fishery enhancement hatcheries on wild populations of salmon. Adv Mar Biol 53:61–194

    Article  PubMed  Google Scholar 

  • Nesler T, Bennett C, Melby J et al (1999) Inventory and status of Arkansas River native fishes in Colorado. Colorado Springs

  • Neuwald JL, Templeton AR (2013) Genetic restoration in the eastern collared lizard under prescribed woodland burning. Mol Ecol 22:3666–3679

    Article  PubMed  Google Scholar 

  • Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution (NY) 51:354–362

    Article  Google Scholar 

  • Nunney L, Campbell K (1993) Assessing minimum population size: demography meets population genetics. Trends Ecol Evol 8:234–239

    Article  CAS  PubMed  Google Scholar 

  • Page LM (1983) Handbook of darters. TFH Publications, Neptune City, New Jersey

    Google Scholar 

  • Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16

    Article  PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Proebstel DS, Martinez AM, Ellis RP (1996) Taxonomic status of cutthroat trout, Rio Grande suckers, and Arkansas darters determined through morphometric, meristic, and mitochondrial DNA analysis. Fort Collins

  • Pulliam HR (1988) Sources, sinks, and population regulation. Am Nat 132:652–661

    Article  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 

  • Rousset F, De S, Montpellier U, Bataillon PE (2008) GENEPOP’ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol 8:103–106

    Article  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M et al (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 45:491–494

    Article  Google Scholar 

  • Samson FB, Knopf FL, Ostlie WR (2004) Great Plains ecosystems: past, present, and future. Wildl Soc Bull 32:6–15

    Article  Google Scholar 

  • Santamaría L, Méndez PF (2012) Evolution in biodiversity policy—current gaps and future needs. Evol Appl 5:202–218

    Article  PubMed Central  Google Scholar 

  • Smith RK, Fausch KD (1997) Thermal tolerance and vegetation preference of Arkansas darter and johnny darter from Colorado plains streams. T Am Fish Soc 126:676–686

    Article  Google Scholar 

  • Sterling KA, Reed DH, Noonan BP, Warren ML (2012) Genetic effects of habitat fragmentation and population isolation on Etheostoma raneyi (Percidae). Conserv Genet 13:859–872

    Article  Google Scholar 

  • Taber CA, Taber BA, Topping MS (1986) Population structure, growth and reproduction of the Arkansas darter, Etheostoma cragini (Percidae). Southwest Nat 31:207–214

    Article  Google Scholar 

  • Tallmon D, Koyuk A, Luikart G, Beaumont M (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301

    Article  PubMed  Google Scholar 

  • Tonnis BD (2006) Microsatellite DNA markers for the rainbow darter, Etheostoma caeruleum (Percidae), and their potential utility for other darter species. Mol Ecol Notes 4:230–232

    Article  Google Scholar 

  • Unmack PJ (2001) Fish persistence and fluvial geomorphology in central Australia. J Arid Environ 49:653–669

    Article  Google Scholar 

  • van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in nonequilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  • Vander Wal E, Garant D, Festa-Bianchet M, Pelletier F (2013) Evolutionary rescue in vertebrates: evidence, applications and uncertainty. Philos Trans R Soc Lond B Biol Sci 368:20120090

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  PubMed  Google Scholar 

  • Willi Y, Van Buskirk J, Hoffman AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Syst 37:433–458

    Article  Google Scholar 

  • Winter TC (2007) The role of ground water in generating streamflow in headwater streams and in maintaining base flow. J Am Water Resour Assoc 43:15–25

    Article  Google Scholar 

Download references

Acknowledgments

We thank E. Bianchi, R. Clawges, M. Cowden, D. Follett, P. Foutz, M. Haworth, W. Massure, J. Ramsay, R. Scarpino, K. Smith, and Z. Underwood for assistance in the field; K. Pearson for data management; and J. Marrinan, T. Mix, and D. Westerman for assistance with tissue collection at NASRF. We thank the Funk-Hoke Lab, K. Bestgen, J. Lepak, M.A. Murphy, J.M. Robertson, J. Smith, and S. Sheth for providing helpful suggestions that improved this study. This research was funded by the Great Plains Landscape Conservation Cooperative and Colorado Parks and Wildlife. S.W.F. was supported by a NSF graduate research fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. W. Fitzpatrick.

Additional information

Data Accessibility Sampling locations, environmental data, and microsatellite genotypes are formatted for entry in Dryad Digital Repository, but have not yet been submitted.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 167 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fitzpatrick, S.W., Crockett, H. & Funk, W.C. Water availability strongly impacts population genetic patterns of an imperiled Great Plains endemic fish. Conserv Genet 15, 771–788 (2014). https://doi.org/10.1007/s10592-014-0577-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0577-0

Keywords

Navigation