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Consistent loss of genetic diversity in isolated cutthroat trout populations independent of habitat size and quality

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Abstract

Fragmentation and isolation of wildlife populations has reduced genetic diversity worldwide, leaving many populations vulnerable to inbreeding depression and local extinction. Nonetheless, isolation is protecting many native aquatic species from interactions with invasive species, often making reconnection an unrealistic conservation strategy. Isolation management is widely used to protect extant cutthroat trout (Oncorhynchus clarkii) populations from invasive species. Despite this, few studies have empirically examined how predictor variables including habitat length, population size, time since isolation and habitat quality, relate to levels of genetic diversity in isolated trout populations. We compared allelic richness of cutthroat trout across 14 microsatellite loci in two connected and 12 anthropogenically isolated populations of the Flathead River basin, Montana. Isolated populations in habitat fragments <8 km stream length had reduced genetic diversity, but diversity was not significantly related to any of our predictor variables. To broaden our scope, we analyzed seven geologically isolated populations from the same river basin occupying habitat fragments up to 18 km in length. These populations showed reduced diversity, regardless of fragment size. Furthermore, geologically isolated populations had significantly lower average allelic richness compared to streams recently isolated by anthropogenic activities. These results demonstrate a consistent loss of genetic diversity through time in isolated populations, emphasizing the need to explore strategies to minimize risks of inbreeding depression. Testing conservation theory and subsequent assumptions broadly across taxa is necessary to ensure efficacy of conservation efforts.

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References

  • Aarts BGW, Van Den Brink FWB, Nienhuis PH (2004) Habitat loss as the main cause of the slow recovery of fish faunas of regulated large rivers in Europe: the transversal floodplain gradient. River Res Appl 20:3–23

    Article  Google Scholar 

  • Alexander LC, Hawthorne DJ, Palmer MA, Lamp WO (2011) Loss of genetic diversity in the North American mayfly ephemerella invaria associated with deforestation of headwater streams. Freshw Biol 56:1456–1467

    Article  Google Scholar 

  • Allendorf F, Luikart G (2008) Conservation and genetics of populations. Blackwell Publishing, Oxford

    Google Scholar 

  • Allendorf F, Bayles D, Bottom DL, Currens KP, Frissell CA, Hankin D, Lichatowhich JA, Nehlsen W, Trotter PC, Williams TH (1997) Prioritizing Pacific salmon stocks for conservation. Conserv Biol 11:140–152

    Article  Google Scholar 

  • Bear EA, McMahon TE (2007) Comparative thermal requirements of westslope cutthroat trout and rainbow trout: implications for species interactions and development of thermal protection strandards. Trans Am Fish Soc 136:1113–1121

    Article  Google Scholar 

  • Boyer MC, Muhlfeld CC, Allendorf FW (2008) Rainbow trout (Oncorhynchus mykiss) invasion and the spread of hybridization with native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can J Fish Aquat Sci 65:658–669

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Cairney M, Taggart JB, HØyheim B (2000) Characterization of microsatellite and minisatellite loci in Atlantic salmon (Salmo salar) and cross species amplification in other salmonids. Mol Ecol 9:2175–2178

    Article  CAS  PubMed  Google Scholar 

  • Carim KJ (2013) Evaluating genetic status and management tradeoffs for conservation of cutthroat trout (Onchorhynchus clarkii). Dissertation, University of Montana

  • Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in timber rattlesnakes (Cortalus horridus). Conserv Biol 24:1059–1069

    Article  PubMed  Google Scholar 

  • Corsi MP (2011) Management and life history consequences of hyrbidization between westlope cutthroat trout (Oncorhynchus clarkii lewisi) and rainbow trout (Oncorhynchus mykiss). Dissertation, University of Montana

  • Costello AB, Down TE, Pollard SM, Pacas CJ, Taylor EB (2003) The influence of history and contemporary stream hydrology on the evolution of genetic diversity within species: an examination of microsatellite DNA variation in Bull Trout, Salvelinus confluentus (Pisces: Salmonidae). Evolution 57:328–344

    Article  CAS  PubMed  Google Scholar 

  • Dixon J, Oli M, Wooten M, Eason T, McCown JW, Cunningham M (2007) Genetic consequences of habitat fragmentation and loss: the case of the Florida black bear (Ursus americanus floridanus). Conserv Genet 8:455–464

    Article  Google Scholar 

  • Downs CC, White RG, Shepard BB (1997) Age at sexual maturity, sex ratio, fecundity, and longevity of isolated headwater populations of westslope cutthroat trout. N Am J Fish Manag 17:85–92

    Article  Google Scholar 

  • Drinan DP, Zale AV, Webb MA, Taper ML, Shepard BB, Kalinowski ST (2012) Evidence of local adaptation in westslope cutthroat trout. Trans Am Fish Soc 141:872–880

    Article  Google Scholar 

  • Dunham JB, Rieman BE (1999) Metapopulation structure of bull trout: influences of physical, biotic and geometrical landscape characteristics. Ecol Appl 9:642–655

    Article  Google Scholar 

  • Dunham JB, Vinyard GL, Rieman BE (1997) Habitat fragmentation and extinction risk of lahontan cutthroat trout. N Am J Fish Manag 17:1126–1133

    Article  Google Scholar 

  • Dunham JB, Adams SB, Schroeter RE, Novinger DC (2002) Alien invasions in aquatic ecosystems: towards an understanding of brook trout invasions and potential impacts on inland cutthroat trout in western North America. Rev Fish Biol Fish 12:373–391

    Article  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fausch KD, Rieman BE, Young MK, Dunham JB (2006) Strategies for conserving native salmonid populations at risk from non-native fish invasions: tradeoffs in using barriers to upstream movement. Rocky Mountain Research Station UFSRMR, Fort Collins

    Google Scholar 

  • Fausch KD, Rieman BE, Dunham JB, Young MK, Peterson DP (2009) Invasion versus isolation: trade-offs in managing native salmonids with barriers to upstream movement. Conserv Biol 23:859–870

    Article  PubMed  Google Scholar 

  • Franklin IR (1980) Evolutionary change in small populations. In: Wilcox BA (ed) Conservation biology: an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 135–149

    Google Scholar 

  • Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404–420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Guy TJ, Gresswell RE, Banks MA (2008) Landscape-scale evlauation of genetic structure among barrier isolated populations of costal cutthroat trout, Oncorhynchus clarki clarki. Can J Fish Aquat Sci 50:1749–1762

    Article  Google Scholar 

  • Hakala J, Hartman K (2004) Drought effect on stream morphology and brook trout (Salvelinus fontinalis) populations in forested headwater streams. Hydrobiologia 515:203–213

    Article  Google Scholar 

  • Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449

    Article  PubMed  Google Scholar 

  • Harig AL, Fausch KD (2002) Minimum habitat requirements for establishing translocated cutthroat trout populations. Ecol Appl 12:535–551

    Article  Google Scholar 

  • Hastings K (2005) Long-term persistence of isolated fish populations in the Alexander Archipelago. Dissertation, University of Montana

  • Hedrick PW, Rashbrook VK, Hedgecock D (2000) Effective population size of winter-run Chinook Salmon based on microsatellite analysis of returning spawners. Can J Fish Aquat Sci 57:2368–2373

    Article  Google Scholar 

  • Hilderbrand RH, Kershner JL (2000) Conserving inland cutthroat trout in small streams—how much is enough? N Am J Fish Manag 20:513–520

    Article  Google Scholar 

  • Holm LE, Brusgaar K (1999) Two polymorphic dinucleotide repeats in rainbow trout (Oncorhynchus mykiss). Anim Genet 30:162–163

    Article  CAS  PubMed  Google Scholar 

  • Horreo JL, Martinez JL, Ayllon F, Pola IG, Monteoliva JA, Heland M, Garcia-Vazquez E (2011) Impact of habitat fragmentation on the genetics of populations in dendritic landscapes. Freshw Biol 56:2567–2579

    Article  Google Scholar 

  • Kitanishi S, Yamamoto T, Edo K, Higashi S (2012) Influences of habitat fragmentation by damming on the genetic structure of masu salmon populations in Hokkaido, Japan. Conserv Genet 13:1017–1026

    Article  Google Scholar 

  • Kritzer JP, Sale PF (2004) Metapopulation ecology in the sea: from Levins’ model to marine ecology and fisheries science. Fish Fish 5:131–140

    Article  Google Scholar 

  • Kruse CG, Hubert WA, Rahel FJ (2000) Status of yellowstone cutthroat trout in wyoming waters. N Am J Fish Manag 20:693–705

    Article  Google Scholar 

  • Kruse CG, Hubert WA, Rahel F (2001) An assessment of headwater isolation as a conservation strategy for cutthroat trout in the Absaroka Mountains of Wyoming. Northwest Sci 75:1–11

    Google Scholar 

  • Lake PS (2000) Disturbance, patchiness, and diversity in streams. J N Am Benthol Soc 19:573–592

    Article  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11:2445–2449

    Article  CAS  PubMed  Google Scholar 

  • Macbeth GM, Broderick D, Buckworth RC, Ovenden JR (2013) Linkage disequilibrium estimation of effective population size with immigrants from divergent populations: a case study on Spanish Mackerel (Scomberomorus commerson). Genes Genomes Genet 3:709–717

    Google Scholar 

  • Miller D, Luce C, Benda L (2003) Time, space, and episodicity of physical disturbance in streams. For Ecol Manag 178:121–140

    Article  Google Scholar 

  • Morita K, Yokota A (2002) Population viability of stream-resident salmonids after habitat fragmentation: a case study with white spotted char (Salvelinus leucomaenis) by an individual based model. Ecol Model 155:85–94

    Article  Google Scholar 

  • Morita K, Morita SA, Yamamoto S (2009) Effects of habitat fragmentation by damming on salmonid fishes: lessons from white spotted charr in Japan. Ecol Res 24:711–722

    Article  Google Scholar 

  • Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf F (2009) Hybridization rapidly reduces the fitness of a native trout in the wild. Biol Lett. doi:10.1098/rsbl.2009.0033

    PubMed  PubMed Central  Google Scholar 

  • Muhlfeld CC, D’Angelo V, Kalinowski ST, Landguth EL, Downs CC, Tohtz J, Kershner JL (2012) A fine-scale assessment of using barriers to conserve native stream Salmonids: a case study in Akokala Creek, Glacier National Park, USA. Open Fish Sci J 5:9–20

    Article  Google Scholar 

  • Nabholz B, Glémin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25:120–130

    Article  CAS  PubMed  Google Scholar 

  • Narum SR, Campbell NR, Meyer KA, Miller MR, Hardy RW (2013) Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Mol Ecol 22:3090–3097

    Article  PubMed  Google Scholar 

  • Nelson RJ, Beacham TD (1999) Isolation and cross species amplification of microatellite loci useful for study of Pacific salmon. Anim Genet 30:228–229

    Article  CAS  PubMed  Google Scholar 

  • Neville H, Dunham JB, Peacock MM (2006) Landscape attributes and life history variability shape genetic structure of trout populations in a stream network. Landsc Ecol 21:901–916

    Article  Google Scholar 

  • Neville H, Dunham JB, Rosenberger A, Umek J, Nelson B (2009) Influences of wildfire, habitat size, and connectivity on trout headwater streams revealed by patterns of genetic diversity. Trans Am Fish Soc 138:1314–1327

    Article  Google Scholar 

  • Novinger DC, Rahel F (2003) Isolation managment with artifical barriers as a conservation strategy for cutthroat trout in headwater streams. Conserv Biol 17:772–781

    Article  Google Scholar 

  • Olsen JB, Bentzen P, Seeb JE (1998) Characterization of seven microsatellite loci derived from pink salmon. Mol Ecol 7:1083–1090

    Article  Google Scholar 

  • Palstra F, 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 

  • Peterson DP, Rieman BE, Dunham JB, Fausch KD, Young MK (2008) Analysis of trade-offs between threats of invasion by non-native brook trout (Salvelinus fontinalis) and intentional isolation for native westslope cutthroat trout (Oncorhynchus clarkii lewisi). Can J Fish Aquat Sci 65:557–573

    Article  Google Scholar 

  • Peterson DP, Rieman BE, Horan DL, Young MK (2013) Patch size but not sort-term isolation influence occurance of westslope cutthroat Trout above human-made barriers. Ecol Freshw Fish. doi:10.1111/eff.12108

    Google Scholar 

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

    Article  Google Scholar 

  • Pierce R, Podner C, Carim K (2013) Response of wild trout to stream restoration over two decades in the Blackfoot River Basin, Montana. Trans Am Fish Soc 142:68–81

    Article  Google Scholar 

  • Pritchard VL, Jones K, Cowley DE (2007) Genetic diversity within fragmented cutthorat trout populations. Trans Am Fish Soc 136:606–623

    Article  Google Scholar 

  • Pujolar JM, Vincenzi S, Zane L, Jesensek D, De Leo GA, Crivelli AJ (2011) The effect of recurrent floods on genetic composition of marble trout populations. PLoS One 6:e23822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Developement Core Team (2012) A language and environment for statistical computing. R foundation for statistical computing, Vienna

  • Rahel FJ (2013) Intentional fragmentation as a management strategy in aquatic systems. Bioscience 63:362–372

    Article  Google Scholar 

  • Resh VH, Brown AV, Covich AP, Gurtz ME, Li HW, Minshall GW, Reice SR, Sheldon AL, Wallace JB, Wissmar RC (1988) The role of disturbance in stream ecology. J N Am Benthol Soc 7:433–455

    Article  Google Scholar 

  • Rexroad E, Coleman RL, Gustafson AL, Hershberger WK, Killefer J (2002) Development of rainbow trout microsatellite markers from repeat enriched libraries. Mar Biotechnol 4:12–16

    Article  CAS  PubMed  Google Scholar 

  • Rieman BE, Dunham JB (2000) Metapopulations and salmonids: a synthesis of life history patterns and emperical observations. Ecol Freshw Fish 9:51–64

    Article  Google Scholar 

  • Roghair CN, Dolloff CA, Underwood MK (2002) Response of a brook trout population and instream habitat to a catastrophic flood and debris flow. Trans Am Fish Soc 131:718–730

    Article  Google Scholar 

  • Sato T, Gwo J-C (2011) Demographic and genetic consequences of population subdivision in Formosa land-locked salmon Oncorhynchus masou formosanus, the southernmost subspecies of the salmonids. Ichthyol Res 58:209–216

    Article  Google Scholar 

  • Shepard BB, Sanborn BW, Ulmer L, Lee DC (1997) Status and risk of extinction for westslope cutthroat trout in the Upper Missouri River Basin, Montana. N Am J Fish Manag 17:1158–1172

    Article  Google Scholar 

  • Shepard BB, May BE, Urie W (2005) Status and conservation of westslope cutthroat within the Western United States. N Am J Fish Manag 25:1426–1440

    Article  Google Scholar 

  • Small MP, Beacham TD, Withler RE, Nelson RJ (1998) Descriminating coho salmon (Oncorhynchus kisutch) populations within the Fraser River, British Columbia, using microsatellite DNA markers. Mol Ecol 7:141–155

    Article  CAS  Google Scholar 

  • Smith CT, Koop BF, Nelson JR (1998) Isolation and characterization of coho salmon (Oncorhynchus kisutch) microsatellite and their use in other salmonids. Mol Ecol 7:1614–1616

    CAS  PubMed  Google Scholar 

  • Spies B, Brasier DJ, O’Reilly PTL, Seamons TR, Bentzen P (2005) Development and characterization of novel tetra-, tri-, and dinucleotide markers in rainbow trout (Oncorhynchus mykiss). Mol Ecol Notes 5:278–281

    Article  CAS  Google Scholar 

  • Steinberg EK, Lindner KR, Gallea J, Maxwell A, Meng J, Allendorf FW (2002) Rates and patterns of microsatellite mutations in pink salmon. Mol Biol Evol 19:1198–1202

    Article  CAS  PubMed  Google Scholar 

  • Taylor M, Stamford D, Baxter JS (2003) Populaiton subdivision in westslope cutthroat trout (Oncorhynchus clarki lewisi) at the northern periphery of its range: evolutionary inferences and conservation implications. Mol Ecol 12:2609–2622

    Article  CAS  PubMed  Google Scholar 

  • Vranckx GUY, Jacquemyn H, Muys B, Honnay O (2012) Meta-analysis of susceptibility of woody plants to loss of genetic diversity through habitat fragmentation. Conserv Biol 26(2):228–237

    Article  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, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780

    Article  PubMed  PubMed Central  Google Scholar 

  • Whiteley AR, Hastings K, Wenburg JK, Frissell CA, Martin JC, Allendorf FW (2010) Genetic variation and effective population size in isolated populations of coastal cutthroat trout. Conserv Genet 11:1929–1943

    Article  Google Scholar 

  • Whiteley AR, Coombs JA, Hudy M, Robinson Z, Colton AR, Nislow KH, Letcher BH (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquat Sci 70(5):678–688

    Article  Google Scholar 

  • Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49

    Article  PubMed  Google Scholar 

  • Wofford JEB, Gresswell RE, Banks MA (2005) Influence of barriers to movement on within-watershed genetic variation of costal cutthroat trout. Ecol Appl 15:628–637

    Article  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, Volume 2: theory of gene frequencies. University of Chicago Press, Chicago

  • Yamamoto S, Morita K, Koizumi I, Maekawa K (2004) Genetic differentiation of white-spotted charr (Salvelinus leucomaenis) populations after habitat fragmentation: spatial-temporal changes in gene frequencies. Conserv Genet 5:529–538

    Article  CAS  Google Scholar 

  • Young MK, Harig AL (2001) A critique of the recovery of greenback cutthroat trout. Conserv Biol 15:1575–1584

    Article  Google Scholar 

  • Young MK, Guenther-Gloss PM, Ficke AD (2005) Predicting cutthroat trout (Oncorhynchus clarkii) abundance in high-elevation streams: revisiting a model of translocation success. Can J Fish Aquat Sci 62:2399–2408

    Article  Google Scholar 

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Acknowledgments

We thank W. Lowe, D. Patterson, C. Muhlfeld, M. Schwartz, and three anonymous reviewers for feedback on previous versions of this work. We also acknowledge our funding sources for this study, including the Westslope Chapter of Trout Unlimited, P.E.O. Scholars Award, the Confederated Salish and Kootenai Tribes, National Science Foundation Graduate Research Fellowship Program DGE-0809127, and Bonneville Power Administration Grant#199101903 to Montana Fish, Wildlife, and Parks. We would like to thank the many people that aided in data collection and processing of genetic samples, including the field crews with the Confederated Salish and Kootenai Tribes and Montana Fish, Wildlife, and Parks, and Sally Painter, Angela Lodmell and Steve Amish with the University of Montana Conservation Genetics Lab. Finally, we thank Fred Allendorf for guidance with data analysis and interpretation.

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Authors and Affiliations

  1. US Forest Service Rocky Mountain Research Station, National Genomics Center for Wildlife and Fish Conservation, 800 E. Beckwith Ave., Missoula, MT, 59801, USA

    Kellie J. Carim

  2. Wildlife Biology Program, University of Montana, 32 Campus Drive, Missoula, MT, 59812, USA

    Kellie J. Carim & Lisa A. Eby

  3. Confederated Salish and Kootenai Tribes, P.O. Box 278, Pablo, MT, 59855, USA

    Craig A. Barfoot

  4. Montana Fish Wildlife and Parks, 490 North Meridian Rd, Kalispell, MT, 59901, USA

    Kellie J. Carim & Matthew C. Boyer

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  1. Kellie J. Carim
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Correspondence to Kellie J. Carim.

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Carim, K.J., Eby, L.A., Barfoot, C.A. et al. Consistent loss of genetic diversity in isolated cutthroat trout populations independent of habitat size and quality. Conserv Genet 17, 1363–1376 (2016). https://doi.org/10.1007/s10592-016-0867-9

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