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Defining population structure and genetic signatures of decline in the giant gartersnake (Thamnophis gigas): implications for conserving threatened species within highly altered landscapes

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Abstract

Anthropogenic habitat fragmentation can disrupt the ability of species to disperse across landscapes, which can alter the levels and distribution of genetic diversity within populations and negatively impact long-term viability. The giant gartersnake (Thamnophis gigas) is a state and federally threatened species that historically occurred in the wetland habitats of California’s Great Central Valley. Despite the loss of 93 % of historic wetlands throughout the Central Valley, giant gartersnakes continue to persist in relatively small, isolated patches of highly modified agricultural wetlands. Gathering information regarding genetic diversity and effective population size represents an essential component for conservation management programs aimed at this species. Previous mitochondrial sequence studies have revealed historical patterns of differentiation, yet little is known about contemporary population structure and diversity. On the basis of 15 microsatellite loci, we estimate population structure and compare indices of genetic diversity among populations spanning seven drainage basins within the Central Valley. We sought to understand how habitat loss may have affected genetic differentiation, genetic diversity and effective population size, and what these patterns suggest in terms of management and restoration actions. We recovered five genetic clusters that were consistent with regional drainage basins, although three northern basins within the Sacramento Valley formed a single genetic cluster. Our results show that northern drainage basin populations have higher connectivity than among central and southern basins populations, and that greater differentiation exists among the more geographically isolated populations in the central and southern portion of the species’ range. Genetic diversity measures among basins were significantly different, and were generally lower in southern basin populations. Levels of inbreeding and evidence of population bottlenecks were detected in about half the populations we sampled, and effective population size estimates were well below recommended minimum thresholds to avoid inbreeding. Efforts focused on maintaining and enhancing existing wetlands to facilitate dispersal between basins and increase local effective population sizes may be critical for these otherwise isolated populations.

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References

  • Anderson CD, Gibbs HL, Douglas ME, Holycross AT (2009) Conservation genetics of the desert massasauga rattlesnake (Sistrurus catenatus edwardsii). Copeia 2009:740–747

    Article  Google Scholar 

  • Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460

    Article  PubMed  Google Scholar 

  • Chiucchi JE, Gibbs HL (2010) Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake. Mol Ecol 19:5345–5358

    Article  PubMed  Google Scholar 

  • Clark RW, Brown WS, Stechert R, Zamudio KR (2008) Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula. Mol Ecol 17:719–730

    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 

  • Dickert C (2005) Giant garter snake surveys at some areas of historic occupation in the grassland ecological area, Merced County, and Mendota Wildlife Area, Fresno County, Califorina. Calif Fish Game 91:255–269

    Google Scholar 

  • Earl D, vonHoldt B (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 

  • Engstrom TN (2010) Genetic analysis of giant garter snake (Thamnophis gigas) populations in the San Joaquin and Sacramento Valleys. Prepared for the Central Valley Project Conservation Program/Habitat Restoration Program

  • 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, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fahig L (1997) Relative effects of habitat loss and fragmentation on species extinction. J Wildl Manag 61:603–610

    Article  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280

    Article  Google Scholar 

  • Fitch H (1941) The feeding habits of California garter snakes. Calif Fish Game 27:2–32

    Google Scholar 

  • Forman R et al (2003) Road ecology: science and solutions. Island Press, Washington DC

    Google Scholar 

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

    Article  Google Scholar 

  • Frankham R, Ralls K (1998) Conservation biology: inbreeding leads to extinction. Nature 392:441–442

    Article  CAS  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  • Frayer WE, Peters DD, Pywell HR (1989) Wetlands of the Califorina Central Valley: status and trends 1939 to mid-1980s. US Fish and Wildlife Service Report, Portland

    Google Scholar 

  • Garone P (2007) The fall and rise of the wetlands of California’s Great Central Valley: a historical and ecological study of an endangered resource of the Pacific Flyway. University of California Press, Berkeley

    Google Scholar 

  • Gates PW (1975) Public land disposal in California. Agric Hist 49:158–178

    Google Scholar 

  • Gautschi B, Widmer A, Joshi J, Koella J (2002) Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. Conserv Genet 3:235–245

    Article  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Guillot G, Leblois R, Coulon A, Frantz AC (2009) Statistical methods in spatial genetics. Mol Ecol 18:4734–4756

    Article  PubMed  Google Scholar 

  • Halstead BJ, Wylie GD, Casazza ML (2010) Habitat suitability and conservation of the giant gartersnake (Thamnophis gigas) in the Sacramento Valley of California. Copeia 2010:591–599

    Article  Google Scholar 

  • Hansen GE (1988) Review of the status of the giant garter snake (Thamnophis couchi gigas) and it supporting habitat. Final Report for California Department of Fish and Game Standard Agreement No C-2060

  • Hansen EC (2008) Implementation of priority 1, priority 2, and priority 3 recovery tasks for giant garter snake (Thamnophis gigas)—continuing surveys in Merced County, California, with an expansion to northern Fresno County. Report prepared for the US Fish and Wildlife Service pursuant to FWS Agreement No 802707G112, 15 April 2008

  • Hansen GE, Brode JM (1980) Status of the giant garter snake, Thamnophis couchii gigas. Inland Fish Endanger Species Progr Spec Publ 80–5:1–14

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  • Jamieson IG, Allendorf FW (2012) How does the 50/500 rule apply to MVPs? Trends Ecol Evol 27:578–584

    Article  PubMed  Google Scholar 

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13

    Article  PubMed Central  PubMed  Google Scholar 

  • Kuchler AW (1977) The map of the natural vegetation of California. University of Kansas, Lawrence

    Google Scholar 

  • Leblois R, Estoup A, Streiff R (2006) Genetics of recent habitat contraction and reduction in population size: does isolation by distance matter? Mol Ecol 15:3601–3615

    Article  PubMed  Google Scholar 

  • Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118

    Article  Google Scholar 

  • Manier MK, Arnold SJ (2005) Population genetic analysis identifies source–sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis). Mol Ecol 14:3965–3976

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Marshall JC Jr, Kingsbury BA, Minchella DJ (2008) Microsatellite variation, population structure, and bottlenecks in the threatened copperbelly water snake. Conserv Genet 10:465–476

    Article  Google Scholar 

  • Meirmans PG, Van Tienderen PH (2004) Genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794

    Article  Google Scholar 

  • Miller JR, Hobbs RJ (2002) Conservation where people live and work. Conserv Biol 16:330–337

    Article  Google Scholar 

  • Miller W, Wright SJ, Zhang Y, Schuster SC, Hayes VM (2010) Optimization methods for selecting founder individuals for captive breeding or reintroduction of endangered species. Pac Symp Biocomput 15:43–53

    Google Scholar 

  • Miller MP, Haig SM, Mullins TD, Popper KJ, Green M (2012) Evidence for population bottlenecks and subtle genetic structure in the yellow rail. The Condor 114:100–112

    Article  Google Scholar 

  • Narum S (2006) Beyond bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York

    Google Scholar 

  • Paquin M, Wylie GD, Routman EJ (2006) Population structure of the giant garter snake, Thamnophis gigas. Conserv Genet 7:25–36

    Article  Google Scholar 

  • Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peery MZ et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418

    Article  PubMed  Google Scholar 

  • Peterson RH (1974) The failure to reclaim: California state swamp land policy and the Sacramento Valley, 1850-1866. South Calif Q 56:45–60

    Article  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 

  • Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective 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 

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

    Google Scholar 

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

    Article  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 

  • Sousa CL, Sloan J (2007) San Joaquin Valley giant garter snake trapping effort 2006. Report prepared for the Califorina Department of Fish and Game, Resource Assessment Program, Los Banos Wildlife Area Publication Number 30

  • Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) COMPUTER PROGRAMS: onesamp: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301

    Article  PubMed  Google Scholar 

  • Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34

    Article  Google Scholar 

  • Tzika AC, Koenig S, Miller R, Garcia G, Remy C, Milinkovitch MC (2008) Population structure of an endemic vulnerable species, the Jamaican boa (Epicrates subflavus). Mol Ecol 17:533–544

    Article  CAS  PubMed  Google Scholar 

  • U. S. Fish and Wildlife Service (2006) Giant garter snake (Thamnophis gigas) 5-year review: summary and evaluation. Sacramento Fish and Wildlife Office, Sacramento, p 46

    Google Scholar 

  • Újvári B, Madsen T, Kotenko T, Olsson M, Shine R, Wittzell H (2002) Low genetic diversity threatens imminent extinction for the Hungarian meadow viper (Vipera ursinii rakosiensis). Biol Conserv 105:127–130

    Article  Google Scholar 

  • U.S. Department of the Interior (1994) The impact of federal programs on wetlands, vol. II, a report to Congress by the Secretary of the Interior. Washington, D. C., March 1994

  • U.S. Fish and Wildlife Service (1993) Endangered and threatened wildlife and plants; determination of threatened status for the giant garter snake. Fed Regist 58:54053–54066

    Google Scholar 

  • Valcarcel PM (2011) Giant Gartersnake spatial ecology in agricultural and constructed wetlands. Masters Thesis, Oregon State University

  • 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 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wylie GD, Amarello MA (2006) Results of 2006 monitoring for giant garter snakes (Thamnophis gigas) for the bank protection project on the left bank of the Colusa Basin drainage canal in Reclamation District 108, Sacramento River Bank Project, Phase II Prepared for the Environmental Planning Section U S Army Corps of Engineers by the US Geological Survey, Biological Resources Division, Dixon Field Station, Dixon, California

  • Wylie GD, Amarello MA (2008) Surveys for the current distribution and abundance of Giant Gartersnakes (Thamnophis gigas) in the southern San Joaquin Valley. Prepared for the US Bureau of Reclamation by the US Geological Survey, Biological Resources Division, Dixon Field Station, Dixon, California:24 pp

  • Wylie G, Hothem R, Bergen D, Martin L, Taylor R, Brussee B (2009) Metals and trace elements in giant garter snakes (Thamnophis gigas) from the Sacramento Valley, California, USA. Arch Environ Contam Toxicol 56:577–587

    Article  CAS  PubMed  Google Scholar 

  • Wylie GD, Casazza ML, Gregory CJ, Halstead BJ (2010) Abundance and Sexual Size dimorphism of the Giant Gartersnake (Thamnophis gigas) in the Sacramento Valley of California. J Herpetol 44:94–103

    Article  Google Scholar 

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Acknowledgments

We wish to thank Tag N. Engstrom for contributing tissues and DNAs from previous studies. We also wish to thank Jimmy Jo Rabbers for his assistance with the copious number of DNA extractions. Finally, we thank Erica Fleishman, Jonathan Richmond, and anonymous reviewers for their comments that greatly improved this manuscript. Support for this project was provided by the Brookfield Natomas LLC and the Western Ecological Research Center. Samples for this project were collected under U.S. Fish and Wildlife Service recovery permit TE-157216-2 and California Scientific Collecting Permit 003004 and accompanying Memorandum of Understanding. Support for tissues collected by the California Department of Fish and Wildlife at Gray Lodge Wildlife Area was provided through an Endangered Species Act Section 6 grant administered by the U.S. Fish and Wildlife Service. This study was approved by the Western Ecological Research Center Animal Care and Use Committee in association with the University of California, Davis. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Correspondence to Dustin A. Wood.

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Wood, D.A., Halstead, B.J., Casazza, M.L. et al. Defining population structure and genetic signatures of decline in the giant gartersnake (Thamnophis gigas): implications for conserving threatened species within highly altered landscapes. Conserv Genet 16, 1025–1039 (2015). https://doi.org/10.1007/s10592-015-0720-6

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