Advertisement

Conservation Genetics

, Volume 15, Issue 1, pp 137–151 | Cite as

Inbreeding and strong population subdivision in an endangered salamander

  • Andrew Storfer
  • Stephen G. Mech
  • Matthew W. Reudink
  • Kristen Lew
Research Article

Abstract

Studies of genetic population structure and genetic diversity are often critical components of endangered species conservation and management plans. Genetic studies are thus particularly important for amphibians, which are in global decline. We studied genetic variation and population structure among 276 individuals from approximately half of the known localities of the endangered Sonora tiger salamander, Ambystoma mavortium stebbinsi, using ten microsatellite loci. Allelic diversity was generally low (2.7 alleles per locus per population) and overall observed heterozygosity (0.191) was significantly lower than expected (0.332). Most populations showed significant departures from Hardy–Weinberg equilibrium, which are likely due to inbreeding. In addition, evidence of recent bottlenecks was suggested by shifted allele frequency distributions in 5 of 16 populations, and ratios of allele number to allele size range (M) values lower than critical values in all populations. A high degree of genetic subdivision (θ = 0.133) was found over all populations, and nearly all pairwise population combinations were genetically subdivided. Thus, gene flow is limited even over small distances, perhaps because high desert grassland throughout the study area limits the efficacy of inter-pond movement of salamanders. Further, population sizes and gene flow of Sonora tiger salamanders are likely compromised by several contemporary ecological threats, including: frequent die-offs due to an infectious virus, introductions of non-native species, and continuing cattle grazing. Overall, these genetic data support the endangered status of the Sonora tiger salamander and suggest the subspecies exists in small, inbred populations.

Keywords

Inbreeding Genetic structure Microsatellites Salamander Ambystoma tigrinum 

Notes

Acknowledgments

We thank R. Ziemba, J. Snyder, M. Myers and C. Steele for help collecting tissue samples. Animals and tissue samples were collected under Arizona State Department of Fish and Game Collecting Permit #SP744166 and US Fish and Wildlife Permit #TE043941-1. This research followed the guidelines of Institutional Animal Care and Use Committees at Arizona State University (#99-670R) and Washington State University (ASAF #3203). This work was supported by US Army Contract #DABT63-99-P-0087 and NSF #0548415 to A.S.

References

  1. Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied-ecology. Ann Rev Ecol Syst 30:133–165CrossRefGoogle Scholar
  2. Banks MA, Eichert W (2000) WHICHRUN (version 3.2) a computer program for population assignment of individuals based on multilocus genotype data. J Hered 91:87–89PubMedCrossRefGoogle Scholar
  3. Beerli P (2002) Migrate-N Documentation and program, part of Lamarc software package. http://popgen.sc.fsu.edu/Migrate/Migrate-n.html. Accessed 29 March 2013
  4. 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 USA 98:4563–4568PubMedCrossRefGoogle Scholar
  5. Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibians. Ecol Lett 5:597–608CrossRefGoogle Scholar
  6. Brunner JL, Schock DM, Davidson EW, Collins JP (2004) Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology 85:560–566CrossRefGoogle Scholar
  7. Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus, Ambystoma tigrinum virus. Dis Aquat Org 77:87–95PubMedCrossRefGoogle Scholar
  8. Collins JP (1981) Distribution, habitats, and life history in the tiger salamander, Ambystoma tigrinum, in east-central and southeast Arizona. Copeia 1981:666–675CrossRefGoogle Scholar
  9. Collins JP, Storfer A (2003) Global amphibian declines: sorting the hypotheses. Divers Dist 9:89–98CrossRefGoogle Scholar
  10. Collins JP, Jones TR, Berna HA (1988) Conserving genetically distinctive populations: the case of the Huachuca tiger salamander (Ambystoma tigrinum stebbinsi). In: Szaro RC, Severson KC, Patton DR (eds) Management of amphibians, reptiles and small mammals in North America. USDA Forest Service GTR-RM-166, Rocky Mountain Forest and Range Experiment Station, Fort Collins, CO, pp 45–53Google Scholar
  11. Collins JP, Brunner JL, Miera V, Parris MJ, Schock DM, Storfer A (2003) Ecology and evolution of infectious disease. In: Semlitsch RD (ed) Amphibian conservation Smithsonian Institution, Washington, DC, p 137–151Google Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. Crowhurst RS, Faries KM, Collantes J, Briggler JT, Koppelman JB, Eggert LS (2011) Genetic relationships of hellbenders in the Ozark highlands of Missouri and conservation implications for the Ozark subspecies (Cryptobranchus alleganiensis bishopi). Conserv Genet 12:637–646CrossRefGoogle Scholar
  14. Curtis JMR, Taylor EB (2004) The genetic structure of coastal giant salamanders (Dicamptodon tenebrosus) in a managed forest. Biol Conserv 115:45–54CrossRefGoogle Scholar
  15. DeMaynadier PG, Hunter ML (1999) Forest canopy closure and juvenile emigration by pond-breeding amphibians in Maine. J Wildl Manag 63:441–450CrossRefGoogle Scholar
  16. Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170PubMedCrossRefGoogle Scholar
  17. Emel SL, Storfer A (2012) A decade of amphibian population genetic studies: synthesis and recommendations. Conserv Genet 13:1685–1689CrossRefGoogle Scholar
  18. 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 10:564–567Google Scholar
  19. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction sites. Genetics 131:479–491PubMedGoogle Scholar
  20. Fitzpatrick BM, Shaffer HB  (2007) Introduction history and habitat variation explain the landscape genetics of hybrid tiger salamanders. Ecol Appl 17:598-608Google Scholar
  21. Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, CambridgeGoogle Scholar
  22. Frankham R (2003) Genetics and conservation biology. Comp Rend Biol 326:S22–S29CrossRefGoogle Scholar
  23. Garner TWJ, Angelone S, Pearman PB (2003) Genetic depletion in Swiss populations of Rana latastei: conservation implications. Biol Conserv 114:371–376CrossRefGoogle Scholar
  24. Garner TWJ, Pearman PB, Angelone S (2004) Genetic diversity across a vertebrate species’ range: a test of the central-peripheral hypothesis. Mol Ecol 13:1047–1053PubMedCrossRefGoogle Scholar
  25. Garza JC (2001) Critical_M.exe software. www.pfeg.noaa.gov/tib/staff/carlos_garcia/carlos%20software.html. Accessed Aug 2007
  26. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  27. Gerst JL (1997) Endangered and threatened wildlife and plants; determination of endangered status for three wetland species found in southern Arizona and northern Sonora, Mexico. Fed Regist 62:665–689Google Scholar
  28. Goldstein DB, Schlötterer C (1999) Microsatellites: evolution and applications. Oxford University Press, OxfordGoogle Scholar
  29. Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Ann N Y Acad Sci 969:323–339PubMedCrossRefGoogle Scholar
  30. Greer AL, Brunner JL, Collins JP (2009) Spatial and temporal patterns of Ambystoma tigrinum virus prevalence in tiger salamanders Ambystoma tigrinum nebulosum. Dis Aquat Org 95:1–6CrossRefGoogle Scholar
  31. Guo SW, Thomson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372PubMedCrossRefGoogle Scholar
  32. Hedrick PW (1995) Gene flow and genetic restoration: the Florida panther as a case study. Conserv Biol 9:995–1007Google Scholar
  33. Hitchings SP, Beebee TJC (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127PubMedCrossRefGoogle Scholar
  34. Hoffman EA, Blouin MS (2004) Historical data refute recent range contraction as cause of low genetic diversity in isolated frog populations. Mol Ecol 13:271–276PubMedCrossRefGoogle Scholar
  35. Jancovich JK, Davidson EW, Morado JF, Jacobs BL, Collins JP (1997) Isolation of a lethal virus from the endangered tiger salamander, Ambystoma tigrinum stebbinsi Lowe. Dis Aquat Org 31:161–167CrossRefGoogle Scholar
  36. Jancovich JK, Mao JH, Chinchar VG et al (2003) Genomic sequence of a ranavirus (family Iridoviridae) associated with salamander mortalities in North America. Virology 316:90–103PubMedCrossRefGoogle Scholar
  37. Jancovich JK, Davidson EW, Parameswaran N, Mao J, Chinchar VG, Collins JP, Jacobs BL, Storfer A (2005) Evidence for emergence of an amphibian disease due to human-enhanced spread. Mol Ecol 14:213–224PubMedCrossRefGoogle Scholar
  38. Jehle R, Arntzen JW (2002) Review: microsatellite markers in amphibian conservation genetics. Herpetol J 12:1–9Google Scholar
  39. Jones TR, Collins JP, Kocher TD, Mitton JB (1988) Systematic status and distribution of Ambystoma tigrinum stebbinsi Lowe (Amphibia: Caudata). Copeia 1988:621–635CrossRefGoogle Scholar
  40. Jones TR, Routman EJ, Begun DJ, Collins JP (1995) Ancestry of an isolated subspecies of salamander, Ambystoma tigrinum stebbinsi Lowe: the evolutionary significance of hybridization. Mol Phylog Evol 4:194–202CrossRefGoogle Scholar
  41. Kats LB, Ferrer RP (2003) Alien predators and amphibian declines. Divers Dist 9:99–110CrossRefGoogle Scholar
  42. Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791CrossRefGoogle Scholar
  43. Lewis PO, Zaykin D (2001). Genetic data analysis: computer program for the analysis of allelic data. Version 1.1. http://lewis.eeb.uconn.edu/lewishome/software.html. Accessed Aug 2007
  44. Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247PubMedCrossRefGoogle Scholar
  45. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998b) Usefulness of molecular markers for detecting bottlenecks via monitoring genetic change. Mol Ecol 7:963–974PubMedCrossRefGoogle Scholar
  46. Madison DM, Farrand L (1998) Habitat use during breeding and emigration in radio implanted tiger salamanders, Ambystoma tigrinum. Copeia 1998:402–410CrossRefGoogle Scholar
  47. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  48. Maret TJ, Snyder JD, Collins JP (2006) Altered drying regime controls distribution of endangered salamanders and introduced predators. Biol Conserv 127:129–138CrossRefGoogle Scholar
  49. Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49Google Scholar
  50. Marshall TC, Slate J, Kruuk L (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655PubMedCrossRefGoogle Scholar
  51. McCallum H (2012) Disease and the dynamics of extinction. Phil Trans R Soc B 367:2828–2839Google Scholar
  52. Mech SG, Storfer A, Ernst JA, Reudink MW, Maloney SC (2003) Polymorphic microsatellite loci for tiger salamanders, Ambystoma tigrinum. Mol Ecol Notes 3:79–81CrossRefGoogle Scholar
  53. Miller D, Gray MJ, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351–2373. doi: 10.3390/v3112351 Google Scholar
  54. Murphy MA, Dezzani R, Pilliod DS, Storfer A (2010) Landscape genetics of high mountain frog metapopulations: an application of gravity models. Mol Ecol 19:3634–3649Google Scholar
  55. Murray KA, Skerratt LF, Speare R et al (2009) Impact and dynamics of disease in species threatened by the chytrid fungus (Batrachochytrium dendrobatidis). Conserv Biol 5:1242–1252CrossRefGoogle Scholar
  56. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  57. Newman RA, Squire T (2001) Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Mol Ecol 10:1087–1100PubMedCrossRefGoogle Scholar
  58. Pechmann JHK, Scott DE, Semlitsch RD et al (1991) Declining amphibian populations: the problem with separating human impacts from natural fluctuations. Science 253:892–895PubMedCrossRefGoogle Scholar
  59. Picco AM, Karam AP, Collins JP (2010) Pathogen host switching in commercial trade with management recommendations. Ecohealth 7:252–256PubMedCrossRefGoogle Scholar
  60. Piry S, Luikart G, Cournet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  61. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  62. Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4:405–410CrossRefGoogle Scholar
  63. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  64. Riley SPD, Shaffer HB, Voss S, Fitzpatrick BM (2003) Hybridization between a rare, native tiger salamander (Ambystoma californiense) and its introduced congener. Ecol Appl 13:1263–1275CrossRefGoogle Scholar
  65. Rothermel BB, Semlitsch RD (2002) An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conserv Biol 16:1324–1332CrossRefGoogle Scholar
  66. Routman E (1993) Population structure and genetic diversity of metamorphic and paedomorphic populations of the tiger salamander, Ambystoma tigrinum. J Evol Biol 6:329–357CrossRefGoogle Scholar
  67. Sabatino SJ, Routman E (2009) Phylogeography and conservation genetics of the hellbender salamander (Cryptobranchus alleganiensis). Conserv Genet 10:1235–1246CrossRefGoogle Scholar
  68. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular Cloning, 2nd edn. Cold Spring Harbor, PlainviewGoogle Scholar
  69. Schloegel LM, Picco AM, Kilpatrick AM et al (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biol Conserv 142:1420–1426CrossRefGoogle Scholar
  70. Schloegel LM, Dazack P, Cunningham AA et al (2010) Two amphibian diseases, chytridiomycosis and ranaviral disease, are now globally notifiable to the World Organization for Animal Health (OIE): an assessment. Dis Aquat Org 92:101–108PubMedCrossRefGoogle Scholar
  71. Schock DM, Bollinger TK, Collins JP (2009) Mortality rates differ among amphibian populations exposed to three strains of a lethal ranavirus. Ecohealth 6:438–448PubMedCrossRefGoogle Scholar
  72. Scribner KT, Arntzen JW, Cruddace N, Oldham RS, Burke T (2001) Environmental correlates of toad abundance and population genetic diversity. Biol Conserv 98:201–210CrossRefGoogle Scholar
  73. Shaffer HB, Breden F (1989) The relationship between allozyme variation and life history: non-transforming salamanders are less variable. Copeia 1989:1016–1023CrossRefGoogle Scholar
  74. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792PubMedCrossRefGoogle Scholar
  75. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462Google Scholar
  76. Smith MA, Green DM (2005) Are all amphibian populations metapopulations? Dispersal and the metapopulation paradigm in amphibian ecology. Ecography 28:110–128CrossRefGoogle Scholar
  77. Spear SF, Peterson CR, Matocq M, Storfer A (2005) Landscape genetics of the blotched tiger salamander, Ambystoma tigrinum melanostictum. Mol Ecol 14:2553–2564PubMedCrossRefGoogle Scholar
  78. Spear SF, Peterson CR, Matocq M, Storfer A (2006) Molecular evidence for recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611CrossRefGoogle Scholar
  79. Spear SF, Storfer A (2008) Landscape genetic structure of tailed frogs in protected versus managed forests. Mol Ecol 17:4642–4656Google Scholar
  80. Storfer A (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180CrossRefGoogle Scholar
  81. Storfer A (2003) Amphibian declines: future directions. Divers Distrib 9:151–163CrossRefGoogle Scholar
  82. Storfer A, Mech SG, Reudink MW, Ziemba RE, Warren JL, Collins JP (2004) Introgression by non-native species in the endangered tiger salamander, Ambystoma tigrinum stebbinsi. Copeia 2004:783–796CrossRefGoogle Scholar
  83. Storfer A, Alfaro MR, Ridenhour BJ, Jancovich JK, Mech SG, Parris MJ, Collins JP (2007) Phylogenetic concordance analysis shows an emerging pathogen is novel and endemic. Ecol Lett 10:1075–1083PubMedCrossRefGoogle Scholar
  84. Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786PubMedCrossRefGoogle Scholar
  85. Summers K, Amos W (1997) Behavioral, ecological and molecular genetic analyses of dart-poison frog, Dendrobates ventrimaculatus. Behav Ecol 8:260–267CrossRefGoogle Scholar
  86. Trenham PC (2001) Terrestrial habitat use by adult California tiger salamanders. J Herpetol 35:343–346CrossRefGoogle Scholar
  87. Trenham PC, Koenig WD, Shaffer HB (2001) Spatially autocorrelated demography and interpond dispersal in the salamander Ambystoma californiense. Ecology 82:3519–3530Google Scholar
  88. Tyler TJ, Liss WJ, Ganio LM, Larson GL, Hoffman RL, Deimling E, Lomnicky G (1998) Interaction between introduced trout and larval salamanders (Ambystoma macrodactylum) in high elevation lakes. Conserv Biol 12:94–105CrossRefGoogle Scholar
  89. Vitt P, Havene K, Hoegh-Guldberg O (2009) Assisted migration: part of an integrated conservation strategy. Trends Ecol Evol 9:473–474CrossRefGoogle Scholar
  90. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Andrew Storfer
    • 1
  • Stephen G. Mech
    • 1
    • 2
  • Matthew W. Reudink
    • 1
    • 3
  • Kristen Lew
    • 1
  1. 1.School of Biological SciencesWashington State UniversityPullmanUSA
  2. 2.Department of BiologyAlbright CollegeReadingUSA
  3. 3.Department of BiologyThompson Rivers UniversityKamloopsCanada

Personalised recommendations