Skip to main content

Advertisement

Log in

Landscape genetics and genetic structure of the southern torrent salamander, Rhyacotriton variegatus

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

Abstract

Landscape genetic methods can be used to identify the most effective conservation measures to maintain functional connectivity among populations. Analyses of habitat factors that facilitate or restrict gene flow are particularly useful for species with specific habitat requirements and low dispersal rates. Rhyacotriton variegatus is a salamander species with low desiccation tolerance and a restricted geographic range, limited to the Pacific Northwest. Thus, we predicted that genetic distance would be positively correlated with climate and landscape variables that increase risk of desiccation. Two genetic distance measures, pairwise FST and proportion of shared alleles (DPS), suggested that gene flow was low among 19 sampling localities (367 total individuals) and genetic structure was high overall (DPS = 0.636 ± 0.010, FST = 0.330 ± 0.011; mean ± SD). Using both least-cost path and Circuitscape models of landscape resistance, we found that low stream cover, low canopy cover, high heat-load index, and short frost-free period all restricted gene flow among populations. We suggest that the conservation status of this species be revisited given this evidence of high genetic structure within the species, the level of habitat fragmentation in their range, and their reliance on dense canopy cover for dispersal. Maintaining stream corridors with buffers of dense canopy cover may maximize connectivity despite the pressures of timber harvest and urbanization.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Adams MJ, Bury RB (2002) The endemic headwater stream amphibians of the American Northwest: associations with environmental gradients in a large forested preserve. Glob Ecol Biogeogr 11:169–178

    Article  Google Scholar 

  • Alp M, Keller I, Westram AM, Robinson CT (2012) How river structure and biological traits influence gene flow: a population genetic study of two stream invertebrates with differing dispersal abilities. Freshw Biol 57:969–981

    Article  Google Scholar 

  • Andersen LW, Fog K, Damgaard C (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc R Soc B 271:1293–1302. doi:10.1098/rspb.2004.2720

    Article  PubMed Central  PubMed  Google Scholar 

  • Anderson CD, Epperson BK, Fortin M-J et al (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575. doi:10.1111/j.1365-294X.2010.04757.x

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. http://CRAN.R-project.org/package=lme4.  Accessed 24 Feb 2014

  • Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology. Biol Conserv 125:271–285

    Article  Google Scholar 

  • Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Advances in molecular ecology. IOS Press, Amsterdam, pp 39–53

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci 98:4563–4568

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bonferroni C (1936) Teoria statistica delle classi e calcolo delle probabilita. Publ R Ist Super Sci Econ Commer Firenze 8:3–62

    Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J et al (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  CAS  PubMed  Google Scholar 

  • Bury RB, Adams MJ (2000) Inventory and monitoring of amphibians in North Cascades and Olympic National Parks, 1995–1998. USGS Forest and Rangeland Ecosystem Science Center

  • California Natural Diversity Database (2011) Special Animals (898 taxa). Biogeographic Data Branch, Department of Fish and Game, The Natural Resources Agency, State of California

  • Campbell Grant EH, Nichols JD, Lowe WH, Fagan WF (2010) Use of multiple dispersal pathways facilitates amphibian persistence in stream networks. Proc Natl Acad Sci 107:6936–6940

    Article  PubMed Central  PubMed  Google Scholar 

  • Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi:10.1093/molbev/msl191

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Connor T, Siren J et al (2013) Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 30:1224–1228. doi:10.1093/molbev/mst028

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for regression relationships between distance matrices: Estimating gene flow with distance. J Agric Biol Environ Stat 7:361–372. doi:10.1198/108571102320

    Article  Google Scholar 

  • Corander J, Siren J, Arjas E (2007) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129

    Article  Google Scholar 

  • Corn PS, Bury RB (1989) Logging in Western Oregon: responses of headwater habitats and stream amphibians. For Ecol Manag 29:39–57

    Article  Google Scholar 

  • Corn PS, Bury RB (1991) Terrestrial amphibian communities in the Oregon Coast Range. General Technical Report PNW-GTR-285. Department of Agriculture, Forest Service, Pacific Northwest Research Station, pp 305–307

  • Coulon A, Cosson JF, Angibault JM et al (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach. Mol Ecol 13:2841–2850

    Article  CAS  PubMed  Google Scholar 

  • Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:231–240

    Article  Google Scholar 

  • Cushman SA, Lewis JS (2010) Movement behavior explains genetic differentiation in American black bears. Landsc Ecol 25:1613–1625

    Article  Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci 91:3166–3170

    Article  PubMed Central  PubMed  Google Scholar 

  • Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

    Article  CAS  Google Scholar 

  • Diller LV, Wallace RL (1996) Distribution and habitat of Rhyacotriton variegatus in managed, young growth forests in north coastal California. J Herpetol 30:184–191

    Article  Google Scholar 

  • Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Conserv 142:1560–1569. doi:10.1016/j.biocon.2008.11.016

    Article  Google Scholar 

  • Emel SL, Storfer A (2012) A decade of amphibian population genetic studies: synthesis and recommendations. Conserv Genet 13:1685–1689. doi:10.1007/s10592-012-0407-1

    Article  Google Scholar 

  • Emel SL, Storfer A (2014) Characterization of 10 microsatellite markers for the southern torrent salamander (Rhyacotriton variegatus). Conserv Genet Resour. doi:10.1007/s12686-014-0230-8

  • Estoup A (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In: Advances in molecular ecology. NATO press, Amsterdam, pp 55–86

  • Etherington TR (2010) Python based GIS tools for landscape genetics: visualising genetic relatedness and measuring landscape connectivity. Methods Ecol Evol 2:52–55. doi:10.1111/j.2041-210X.2010.00048.x

    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. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  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. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) 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 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • Gesch DB (2007) The national elevation dataset. In: Maune D (ed) Digital elevation model technologies and applications: the DEM users manual, 2nd edn. American Society for Photogrammetry and Remote Sensing, Bethesda, pp 99–118

    Google Scholar 

  • Gesch D, Oimoen M, Greenlee S et al (2002) The national elevation dataset: photogrammetric engineering and remote sensing. J Am Soc Photogramm Remote Sens 68:5–11

    Google Scholar 

  • Goldberg CS, Waits LP (2010) Quantification and reduction of bias from sampling larvae to infer population and landscape genetic structure. Mol Ecol Resour 10:304–313. doi:10.1111/j.1755-0998.2009.02755.x

    Article  PubMed  Google Scholar 

  • Good DA, Wake DB (1992) Geographic Variation and Speciation in the Torrent Salamanders of the Genus Rhyacotriton (Caudata: Rhyacotritonidae). University of California Press, Berkeley

  • Hammerson G (2004) Rhyacotriton kezeri. IUCN Red List of Threatened Species Version 2011.1. http://www.iucnredlist.org. Accessed 17 Jan 2014

  • Hedrick PW, Miller PS (1992) Conservation genetics: techniques and fundamentals. Ecol Appl 2:30–46

    Article  Google Scholar 

  • Homer C, Dewitz J, Fry J et al (2007) Completion of the 2001 national land cover database for the conterminous United States. Progr Eng Remote Sens 73:337–341

    Google Scholar 

  • IUCN, International C, NatureServe (2011) An analysis of amphibians on the 2008 IUCN Red List. http://www.iucnredlist.org/amphibian. Accessed 16 Jan 2014

  • Lannoo M (2006) Amphibian declines: the conservation status of United States species. University of California Press, Berkeley

    Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data (2000) version 1.0

  • Lowe WH, McPeek MA, Likens GE, Cosentino BJ (2008) Linking movement behaviour to dispersal and divergence in plethodontid salamanders. Mol Ecol 17:4459–4469. doi:10.1111/j.1365-294X.2008.03928.x

    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 

  • Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 10:614–621. doi:10.1016/j.tree.2013.05.012

    Article  Google Scholar 

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • McCune B, Keon D (2002) Equations for potential annual direct incident radiation and heat load. J Veg Sci 13:603–606

    Article  Google Scholar 

  • McRae BH, Schumaker NH, McKane RB et al (2008) A multi-model framework for simulating wildlife population response to land-use and climate change. Ecol Model 219:77–91. doi:10.1016/j.ecolmodel.2008.08.001

    Article  Google Scholar 

  • Measey GJ, Galbusera P, Breyne P, Matthysen E (2007) Gene flow in a direct-developing, leaf litter frog between isolated mountains in the Taita Hills, Kenya. Conserv Genet 8:1177–1188. doi:10.1007/s10592-006-9272-0

    Article  Google Scholar 

  • Miller MP, Haig SM, Wagner RS (2006) Phylogeography and spatial genetic structure of the southern torrent salamander: implications for conservation and management. J Hered 97:561–570. doi:10.1093/jhered/esl038

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Neville HL, 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 

  • Nussbaum RA, Tait CK (1977) Aspects of the life history and ecology of the Olympic Salamander, Rhyacotriton olympicus (Gaige). Am Midl Nat 98:176–199

    Article  Google Scholar 

  • Olson DH, Anderson PD, Frissell CA et al (2007) Biodiversity management approaches for stream–riparian areas: perspectives for Pacific Northwest headwater forests, microclimates, and amphibians. For Ecol Manag 246:81–107. doi:10.1016/j.foreco.2007.03.053

    Article  Google Scholar 

  • Petranka JW (1998) Rhyacotriton variegatus Stebbins and Lowe Southern torrent salamander. In: Salamanders of the United States and Canada. Smithsonian Institution Press, Washington DC, pp 441–443

  • Pimm SL, Raven PR (2000) Biodiversity: extinction by the numbers. Nature 403:843–845. doi:10.1038/35002708

    Article  CAS  PubMed  Google Scholar 

  • Piry S, Luikart G, Cornuet J-M (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 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/. Accessed 23 Jan 2014

  • Ray C (1958) Vital limits and rates of desiccation in salamanders. Ecology 39:75–83

    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 

  • Rehfeldt GE (2006) A spline model of climate for the western United States. General Technical Report, Rocky Mountain Research Station, U.S. Forest Service

  • Richards-Zawacki CL (2009) Effects of slope and riparian habitat connectivity on gene flow in an endangered Panamanian frog, Atelopus varius. Divers Distrib 15:796–806. doi:10.1111/j.1472-4642.2009.00582.x

    Article  Google Scholar 

  • Rochelle JA, Lehmann LA, Wisnewski J (1999) Forest Fragmentation: wildlife and management implications. Brill Academic Publishers, Boston

    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. doi:10.1111/j.1471-8286.2007.01931.x

    Article  PubMed  Google Scholar 

  • Schlötterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365–371

    Article  PubMed  Google Scholar 

  • Segelbacher G, Cushman SA, Epperson BK et al (2010) Applications of landscape genetics in conservation biology: concepts and challenges. Conserv Genet 11:375–385. doi:10.1007/s10592-009-0044-5

    Article  Google Scholar 

  • Spear SF, Storfer A (2008) Landscape genetic structure of coastal tailed frogs (Ascaphus truei) in protected vs. managed forests. Mol Ecol 17:4642–4656

    Article  PubMed  Google Scholar 

  • Spear SF, Storfer A (2010) Anthropogenic and natural disturbance lead to differing patterns of gene flow in the Rocky Mountain tailed frog, Ascaphus montanus. Biol Conserv 143:778–786

    Article  Google Scholar 

  • Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscape genetics of the blotched tiger salamander (Ambystoma tigrinum melanostictum). Mol Ecol 14:2553–2564. doi:10.1111/j.1365-294X.2005.02573.x

    Article  CAS  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Evans JS et al (2007) Putting the “landscape” in landscape genetics. Heredity 98:128–142

    Article  CAS  PubMed  Google Scholar 

  • Storfer A, Murphy MA, Spear SF et al (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514

    Article  PubMed  Google Scholar 

  • StreamNet GIS Data (2003) Metadata for Pacific Northwest coho salmon fish distribution spatial data set. Portland (OR): StreamNet, May 2003. http://www.streamnet.org/online-data/GISData.html. Accessed 16 Jan 2014

  • Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Trumbo DR, Spear SF, Baumsteiger J, Storfer A (2013) Rangewide landscape genetics of an endemic Pacific northwestern salamander. Mol Ecol 22:1250–1266. doi:10.1111/mec.12168

    Article  PubMed  Google Scholar 

  • van Strien MJ, Keller D, Holderegger R (2012) A new analytical approach to landscape genetic modelling: least-cost transect analysis and linear mixed models. Mol Ecol 21:4010–4023. doi:10.1111/j.1365-294X.2012.05687.x

    Article  Google Scholar 

  • Wagner HH, Fortin M-J (2010) Spatial analysis of landscapes: concept and statistics. Ecology 86:1975–1987

    Article  Google Scholar 

  • Wagner RS, Miller MP, Haig SM (2006) Phylogeography and genetic identification of newly-discovered populations of torrent salamanders (Rhyacotriton cascadae and R. variegatus) in the central Cascades (USA). Herpetologica 62:63–70

    Article  Google Scholar 

  • Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genetics 166:1963–1979

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594. doi:10.1534/genetics.108.100214

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang IJ, Savage WK, Shaffer HB (2009) Landscape genetics and least-cost path analysis reveal unexpected dispersal routes in the California tiger salamander (Ambystoma californiense). Mol Ecol 18:1365–1374. doi:10.1111/j.1365-294X.2009.04122.x

    Article  PubMed  Google Scholar 

  • Welsh HH Jr (1990) Relictual amphibians and old-growth forests. Conserv Biol 4:309–319

    Article  Google Scholar 

  • Welsh HH Jr, Lind AJ (1991) The structure of the herpetofaunal assemblage in the douglas-fir/hardwood forests of northwestern California and southwestern Oregon. Department of Agriculture, Forest Service, Pacific Northwest Research Station, pp 394–458

  • Welsh HH Jr, Lind AJ (1992) Population ecology of two relictual salamanders from the Klamath Mountains of Northwestern California. In: McCullough DR, Barrett RH (eds) Wildlife 2001: populations. Elsevier Applied Science, London, pp 419–437

    Chapter  Google Scholar 

  • Welsh HH Jr, Lind AJ (1996) Habitat correlates of the southern torrent salamander. J Herpetol 30:385–398

    Article  Google Scholar 

  • Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST ≠ 1/(4Nm + 1). Heredity 82:117–125

    Article  PubMed  Google Scholar 

  • Willy A (1995) Endangered and threatened wildlife and plants; 90-day finding for a petition to list the southern torrent salamander. Fed Reg 60:33785–33786

    Google Scholar 

  • Wright S (1931) Evolution in mendelian populations. Genetics 31:39–59

    Google Scholar 

Download references

Acknowledgments

We would like to thank the American Museum of Natural History Theodore Roosevelt Memorial Fund, Sigma Xi Grants-in-Aid of Research, and the Washington State University Elling Foundation for funding the project. M. Adams, A. Caldwell, E. Dunn, K. Emel, Z. Emel, B. Hogberg, and J. Miller assisted with tissue collection. P. Frias, R. M. Larios, S. Micheletti, S. Spear, D. Trumbo, and G. Zancoli provided guidance with laboratory and computer analyses. Finally, we thank B. Epstein, S. Micheletti, L. Shipley, D. Trumbo, and L. Waits for providing comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sarah L. Emel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 158 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Emel, S.L., Storfer, A. Landscape genetics and genetic structure of the southern torrent salamander, Rhyacotriton variegatus . Conserv Genet 16, 209–221 (2015). https://doi.org/10.1007/s10592-014-0653-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0653-5

Keywords

Navigation