Abstract
Genetic population structure was evaluated for the White Sands pupfish (Cyprinodon tularosa), a protected fish species comprised of two Evolutionarily Significant Units (ESUs); the Malpais Spring ESU and the Salt Creek ESU. The Malpais Spring ESU is restricted to Malpais Spring, whereas the Salt Creek ESU includes the native Salt Creek population and two Salt Creek-derived populations at Mound Spring and Lost River; all three of these habitats are physically fragmented. We sampled the upper and lower reaches of the four populations, examining 13 DNA microsatellite loci from 40 individuals per population. As expected, significant genetic structure was observed between the two ESUs; Malpais Spring and Salt Creek. Substantial genetic drift was observed for the introduced Lost River population, with modest genetic drift for the introduced Mound Spring population. Taken together with ecological data, neither of the introduced populations successfully replicates the Salt Creek population. We also report significant reductions in genetic diversity for the upper reaches of both Salt Creek and Lost River, indicating that recent habitat changes have altered the genetic structure of these two populations. We consider these findings along with previously reported ecological data to develop guidelines for managing C. tularosa.
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References
Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190
Aló D, Turner TF (2005) Effects of habitat fragmentation on effective population size in the endangered Rio Grande silvery minnow. Conserv Biol 19:1138–1148
Benjamini Y, Yekutieli D (2001) The control of false discovery rate under dependency. Ann Stat 29:1165–1188
Burg TM, Wilcox JL, Martin A (2002) Isolation and characterization of polymorphic microsatellite loci in pupfish (genus Cyprinodon). Conserv Genet 3:197–204
Carman S (2010) White Sands pupfish status report, 2009. New Mexico Game and Fish Report, Santa Fe
Castric V, Bonney F, Bernatchez L (2001) Landscape structure and hierarchical genetic diversity in the brook charr, Salvelinus fontinalis. Evolution 55:1016–1028
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
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 (Cyrpinodon tularosa). Ecol Res 22:902–910
Collyer ML, Heilveil JS, Stockwell CA (2011) Contemporary evolutionary divergence for a protected species following assisted colonization. PLoS One 6:e22310. doi:10.1371/journal.pone.0022310
Costello AB, Down TE, Pollard SM, Pacas CJ (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
Crispo E, Bentzen P, Reznick DN, Kinnison MT, Hendry AP (2006) The relative influence of natural selection and geography on gene flow in guppies. Mol Ecol 15:49–62. doi:10.1111/j.1365-294X.2005.02764.x
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
Dunham JB, Minckley WL (1998) Allozymic variation in desert pupfish from natural and artificial habitats: genetic conservation in fluctuating populations. Biol Conserv 84:7–15
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
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 Bioinformatics Online 1:47–50
Finger AJ, Parmenter S, May BP (2013) Conservation of the Owens pupfish: genetic effects of multiple translocations and extirpations. T Am Fish Soc 142:1430–1443
Frankham R (1995) Inbreeding and extinction: a threshold effect. Conserv Biol 9:792–799
Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443
Hendry AP, Taylor EB, McPhail JD (2002) Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the misty system. Evolution 56:1199–1216
Iyengar A, Stockwell CA, Layfield D, Morin PA (2004) Characterization of microsatellite markers in a threatened species, the White Sands pupfish (Cyprinodon tularosa). Mol Ecol Notes 4:191–193
Jester DB, Suminski RR (1982) Age and growth, fecundity, abundance, and biomass production of the White Sands pupfish, Cyprinodon tularosa (Cyprinodontidae), in a desert pond. Southwest Nat 27:43–54
Keller I, Largiader CR (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc R Soc Lond B Biol Sci 270:417–423
Koike H, Echelle AA, Loftis D, Van Den Bussche RA (2008) Microsatellite DNA analysis of success in conserving genetic diversity after 33 years of refuge management for the desert pupfish complex. Anim Conserv 11:321–329
Leberg PL (1993) Strategies for population reintroduction: effects of genetic variability on population growth and size. Conserv Biol 7:194–199
Martin AP, Wilcox JL (2004) Evolutionary history of ash meadows pupfish (genus Cyprinodon) populations inferred using microsatellite markers. Conserv Genet 5:769–782
Miller RR, Echelle AA (1975) Cyprinodon tularosa, a new cyprinodontid fish from the Tularosa Basin, New Mexico. Southwest Nat 19:365–377
Mills LS, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518
Minckley WL (1995) Translocation as a tool for conserving imperiled fishes: experiences in western United States. Biol Conserv 72:297–309
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Neraas LP, Spruell P (2001) Fragmentation of riverine systems: the genetic effects of dams on bull trout (Salvelinus confluentus) in the Clark Fork River system. Mol Ecol 10:1153–1164
Parker KM, Sheffer RJ, Hedrick PW (1999) Molecular variation and evolutionarily significant units in the endangered Gila topminnow. Conserv Biol 13:108–116
Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pittenger JS, Springer CL (1999) Native range and conservation of the White Sands pupfish (Cyprinodon tularosa). Southwest Nat 44:157–165
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure from multilocus genotype data. Genetics 155:945–959
Rogowski DL (2004) Direct, indirect, and potential effects of salinity on the White Sands pupfish (Cyprinodon tularosa). Doctoral Dissertation, North Dakota State University, Fargo
Rogowski D, Stockwell CA (2006) Parasites and salinity: costly tradeoffs in a threatened species. Oecologia 146:615–622
Rogowski DL, Reiser H, Stockwell CA (2006) Fish habitat associations in a spatially variable desert stream. J Fish Biol 68:1473–1483
Smith MW, Smith MH, Chesser RK (1983) Biochemical Genetics of Mosquitofish. I. Environmental Correlates, and Temporal and Spatial Heterogeneity of Allele Frequencies within a River Drainage. Copeia (1):182
Stockwell CA, Mulvey M (1998) Phosphogluconate dehydrogenase polymorphism and salinity in the White Sands pupfish. Evolution 52:1856–1860
Stockwell CA, Mulvey M, Jones AG (1998) Genetic evidence for two evolutionarily significant units of White Sands pupfish. Anim Conserv 1:213–225
Stockwell CA, Heilveil JS, Purcell K (2013) Estimating divergence time for two evolutionarily significant units of a protected fish species. Conserv Genet 14:215–222
Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180
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 3:244–262
Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159
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
Acknowledgements
Special thanks are due to David Layfield for his assistance with collecting these data. The authors would also like to thank Jeanne Dye and Hildegard Reiser (CES/CEV, Holloman AFB) and Robert Myers (Environmental Stewardship, Environmental Division in the Directorate of Public Works, WSMR), for arrangement of range visitation. Janice Terfehr and Makenzie Stockwell assisted with collecting fish. This research was funded by DOD Legacy Resource Program Grant no. DACA87-00-H-0014 administered by H. Reiser and J. Dye, (CES/CEV, Holloman AFB) and North Dakota EPA-STAR EPSCoR Grant to CAS. Pupfish were collected on White Sands Missile Range under New Mexico State collecting permit 2887 and fish were handled and sacrificed following a North Dakota State University Animal Care and Use Committee approved protocol (#A0117). The authors do not have any conflicts of interest concerning the information presented in this manuscript. This manuscript benefitted from comments provided by R. Myers, S. Carman, K. Purcell, Y. Chen and two anonymous reviewers. This paper was approved for public release by White Sands Missile Range; distribution unlimited. OPSEC review completed on 31 March 2009.
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Heilveil, J.S., Stockwell, C.A. Genetic signatures of translocations and habitat fragmentation for two evolutionarily significant units of a protected fish species. Environ Biol Fish 100, 631–638 (2017). https://doi.org/10.1007/s10641-017-0591-4
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DOI: https://doi.org/10.1007/s10641-017-0591-4