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Population genetic structure and disease in montane boreal toads: more heterozygous individuals are more likely to be infected with amphibian chytrid

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Abstract

Amphibians are more threatened than any other vertebrate group, with 41 % of species classified as threatened. The causes of most declines are not well understood, though many declines have been linked to disease. Additionally, amphibians are physiologically constrained to moist habitats and considered poor dispersers; thus, they may suffer genetic consequences of population isolation. To understand threats to the persistence of boreal toads (Bufo boreas) in Glacier National Park, USA, we genotyped 551 individuals at 11 microsatellite loci and used Bayesian clustering methods to describe population genetic structure and identify barriers to gene flow. We found evidence of two primary genetic groups that differed substantially in elevation and two secondary groups within the high elevation group. There was also evidence of further substructure within the southern high elevation group, suggesting mountain ridges are barriers to gene flow at local scales. Overall, genetic variation was high, but allelic richness declined with increasing elevation, reflecting greater isolation or smaller effective population sizes of high altitude populations. We tested for Batrachochytrium dendrobatidis (Bd), the fungal pathogen which causes chytridiomycosis, and we found that 35 of 199 toads were positive for Bd. Unexpectedly, more heterozygous individuals were more likely to be infected. This suggests that dispersal facilitates the spread of disease because heterozygosity may be highest where dispersal and gene flow are greatest.

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References

  • Adams S, Schmetterling D, Young M (2005) Instream movement by boreal toads (Bufo boreas boreas). Herpetol Rev 36:27–33

    Google Scholar 

  • Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190

    Article  Google Scholar 

  • Andreasen V, Christiansen FB (1989) Persistence of an infectious disease in a subdivided population. Math Biosci 96:239–253

    Article  CAS  PubMed  Google Scholar 

  • Annis SL, Dastoor FP, Ziel H et al (2004) A DNA-based assay identifies Batrachochytrium dendrobatidis in amphibians. J Wildl Dis 40:420–428

    Article  CAS  PubMed  Google Scholar 

  • Bartelt PE, Peterson CR, Klaver RW (2004) Sexual differences in the post-breeding movements and habitats selected by western toads (Bufo boreas) in southeastern Idaho. Herpetologica 60:455–467

    Article  Google Scholar 

  • Berger L, Speare R, Daszak P et al (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95:9031–9036

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blaustein AR, Wake DB, Sousa WP (1994) Amphibian declines: judging stability, persistence, and susceptibility of populations to local and global extinctions. Conserv Biol 8:60–71

    Article  Google Scholar 

  • Bonin A, Taberlet P, Miaud C, Pompanon F (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Mol Biol Evol 23:773–783

    Article  CAS  PubMed  Google Scholar 

  • Brown JH, Kodric-Brown A (1977) Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58:445–449

    Article  Google Scholar 

  • Clarke BC (1979) The evolution of genetic diversity. Proc R Soc Lond B 205:453–474

    Article  CAS  PubMed  Google Scholar 

  • Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259–1267

    Article  Google Scholar 

  • Corn PS, Hossack BR, Muths E et al (2005) Status of amphibians on the Continental Divide: surveys on a transect from Montana to Colorado, USA. Alytes 22:85–94

    Google Scholar 

  • Coulon A (2009) Genhet: an easy-to-use R function to estimate individual heterozygosity. Mol Ecol Resour 10:167–169

    Article  PubMed  Google Scholar 

  • Crawford AJ, Lips KR, Bermingham E (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proc Natl Acad Sci USA 107:13777–13782

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Daugherty CH, Sheldon AL (1982) Age-specific movement patterns of the frog Ascaphus truei. Herpetologica 38:468–474

    Google Scholar 

  • Duellman WE, Trueb L (1994) The biology of amphibians. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Epps CW, Palsbøll PJ, Wehausen JD et al (2005) Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038

    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

    Article  CAS  PubMed  Google Scholar 

  • Fisher MC, Garner TWJ, Walker SF (2009) Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu Rev Microbiol 63:291–310

    Article  CAS  PubMed  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Funk WC, Blouin MS, Corn PS et al (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496

    Article  CAS  PubMed  Google Scholar 

  • Giordano AR, Ridenhour BJ, Storfer A (2007) The influence of altitude and topography on genetic structure in the long-toed salamander (Ambystoma macrodactulym). Mol Ecol 16:1625–1637

    Article  CAS  PubMed  Google Scholar 

  • Goebel AM, Ranker TA, Corn PS, Olmstead RG (2009) Mitochondrial DNA evolution in the Anaxyrus boreas species group. Mol Phylogenet Evol 50:209–225

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005a) A spatial statistical model for landscape genetics. Genetics 170:1261–1280

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guillot G, Mortier F, Estoup A (2005b) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

    Article  CAS  Google Scholar 

  • Guo SW, Thompson EA (1992) A Monte Carlo method for combined segregation and linkage analysis. Am J Hum Genet 51:1111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hammerson GA, Santos-Barrera G, Muths E (2004) Anaxyrus boreas. IUCN red list of threatened species, version 2012.2. http://www.redlist.org

  • Harcourt AH, Coppeto SA, Parks SA (2002) Rarity, specialization and extinction in primates. J Biogeogr 29:445–456

    Article  Google Scholar 

  • Harris RT (1975) Seasonal activity and microhabitat utilization in Hyla cadaverina (Anura: Hylidae). Herpetologica 31:236–239

    Google Scholar 

  • Hedrick PW, Kim TJ, Parker KM (2001) Parasite resistance and genetic variation in the endangered Gila topminnow. Anim Conserv 4:103–109

    Article  Google Scholar 

  • Hess G (1996) Disease in metapopulation models: implications for conservation. Ecology 77:1617–1632

    Article  Google Scholar 

  • Hethcote HW (1976) Qualitative analyses of communicable disease models. Math Biosci 28:335–356

    Article  Google Scholar 

  • Hoffmann M, Hilton-Taylor C, Angulo A et al (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509

    Article  CAS  PubMed  Google Scholar 

  • Hossack BR, Lowe WH, Corn PS (2013a) Rapid increases and time-lagged declines in amphibian occupancy after wildfire. Conserv Biol 27:219–228

    Article  PubMed  Google Scholar 

  • Hossack BR, Lowe WH, Ware JL, Corn PS (2013b) Disease in a dynamic landscape: host behavior and wildfire reduce amphibian chytrid infection. Biol Conserv 157:293–299

    Article  Google Scholar 

  • Kilpatrick AM, Briggs CJ, Daszak P (2010) The ecology and impact of chytridiomycosis: an emerging disease of amphibians. Trends Ecol Evol 25:109–118

    Article  PubMed  Google Scholar 

  • Kimura M, Maruyama T, Crow JF (1963) The mutation load in small populations. Genetics 48:1303–1312

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kleeberger SR, Werner JK (1982) Home range and homing behavior of Plethodon cinereus in northern Michigan. Copeia 1982:409–415

    Article  Google Scholar 

  • Leung LR, Qian Y, Bian X et al (2004) Mid-century ensemble regional climate change scenarios for the western United States. Clim Change 62:75–113

    Article  Google Scholar 

  • Lips KR, Brem F, Brenes R et al (2006) Emerging infectious disease and the loss of biodiversity in a neotropical amphibian community. Proc Natl Acad Sci USA 103:3165–3170

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lougheed SC, Gascon C, Jones DA et al (1999) Ridges and rivers: a test of competing hypotheses of Amazonian diversification using a dart-poison frog (Epipedobates femoralis). Proc R Soc Lond B 266:1829–1835

    Article  CAS  Google Scholar 

  • Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051

    Article  PubMed  Google Scholar 

  • Lowe WH, Mcpeek MA, Likens GE, Cosentino BJ (2008) Linking movement behaviour to dispersal and divergence in plethodontid salamanders. Mol Ecol 17:4459–4469

    Article  PubMed  Google Scholar 

  • Luikart G, Pilgrim K, Visty J et al (2008) Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep. Biol Lett 4:228–231

    Article  PubMed Central  PubMed  Google Scholar 

  • Luquet E, David P, Lena J-P et al (2011) Heterozygosity–fitness correlations among wild populations of European tree frog (Hyla arborea) detect fixation load. Mol Ecol 20:1877–1887

    Article  CAS  PubMed  Google Scholar 

  • Manier MK, Arnold SJ (2006) Ecological correlates of population genetic structure: a comparative approach using a vertebrate metacommunity. Proc R Soc B 273:3001–3009

    Article  PubMed Central  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 

  • McCauley DE (1991) Genetic consequences of local population extinction and recolonization. Trends Ecol Evol 6:5–8

    Article  CAS  PubMed  Google Scholar 

  • McRae BH, Beier P, Dewald LE et al (2005) Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 14:1965–1977

    Article  CAS  PubMed  Google Scholar 

  • Meagher S (1999) Genetic diversity and Capillaria hepatica (Nematoda) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324

    Article  Google Scholar 

  • Moore JA, Tallmon DA, Nielsen J, Pyare S (2011) Effects of the landscape on boreal toad gene flow: does the pattern–process relationship hold true across distinct landscapes at the northern range margin? Mol Ecol 20:4858–4869

    Article  PubMed  Google Scholar 

  • Mote PW (2006) Climate-driven variability and trends in mountain snowpack in western North America. J Clim 19:6209–6220

    Article  Google Scholar 

  • Murphy MA, Evans JS, Storfer A (2010) Quantifying Bufo boreas connectivity in Yellowstone National Park with landscape genetics. Ecology 91:252–261

    Article  PubMed  Google Scholar 

  • Muths E (2003) Home range and movements of boreal toads in undisturbed habitat. Copeia 2003:160–165

    Article  Google Scholar 

  • Muths E, Stephen Corn P, Pessier AP, Earl Green D (2003) Evidence for disease-related amphibian decline in Colorado. Biol Conserv 110:357–365

    Article  Google Scholar 

  • Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354–362

    Article  Google Scholar 

  • Newman RA, Squire T (2001) Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Mol Ecol 10:1087–1100

    Article  CAS  PubMed  Google Scholar 

  • Nichols D, Lamirande E, Pessier A, Longcore J (2001) Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs. J Wildl Dis 37:1–11

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2005) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pérez-Espona S, Pérez-Barbería FJ, Mcleod JE et al (2008) Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus). Mol Ecol 17:981–996

    Article  PubMed  Google Scholar 

  • Pidancier N, Miquel C, Miaud C (2003) Buccal swabs as a non-destructive tissue sampling method for DNA analysis in amphibians. Herpetol J 13:175–178

    Google Scholar 

  • Pilliod DS, Muths E, Scherer RD et al (2010) Effects of amphibian chytrid fungus on individual survival probability in wild boreal toads. Conserv Biol 24:1259–1267

    Article  PubMed  Google Scholar 

  • Post WM, DeAngelis DL, Travis CC (1983) Endemic disease in environments with spatially heterogeneous host populations. Math Biosci 63:289–302

    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 

  • Purvis A, Jones KE, Mace GM (2000) Extinction. Bioessays 22:1123–1133

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    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 

  • Roelke ME, Martenson JS, O’Brien SJ (1993) The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Curr Biol 3:340–350

    Article  CAS  PubMed  Google Scholar 

  • Ron SR (2005) Predicting the distribution of the amphibian pathogen Batrachochytrium dendrobatidis in the New World. Biotropica 37:209–221

    Article  Google Scholar 

  • Rothermel BB, Semlitsch RD (2002) An experimental investigation of landscape resistance of forest versus old-field habitats to emigrating juvenile amphibians. Conserv Biol 16:1324–1332

    Article  Google Scholar 

  • Saccheri I, Kuussaari M, Kankare M et al (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494

    Article  CAS  Google Scholar 

  • Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci USA 108:16705–16710

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Semlitsch RD (1981) Terrestrial activity and summer home range of the mole salamander (Ambystoma talpoideum). Can J Zool 59:315–322

    Article  Google Scholar 

  • Semlitsch RD, Todd BD, Blomquist SM et al (2009) Effects of timber harvest on amphibian populations: understanding mechanisms from forest experiments. Bioscience 59:853–862

    Article  Google Scholar 

  • Simandle ET, Peacock MM, Zirelli L, Tracy CR (2005) Sixteen microsatellite loci for the Bufo boreas group. Mol Ecol Notes 6:116–119

    Article  Google Scholar 

  • Skerratt L, Berger L, Speare R et al (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4:125–134

    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

    Article  CAS  PubMed  Google Scholar 

  • Spielman D, Brook BW, Briscoe DA, Frankham R (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–448

    Article  Google Scholar 

  • 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 

  • Switzer JF, Johnson R, Lubinski BA, King TL (2009) Genetic structure in the Bufo boreas species group (Anura, Bufonidae): an evaluation of the Southern Rocky Mountain population. United States Fish and Wildlife Service, Mountain-Prairie region

    Google Scholar 

  • Tallmon DA, Funk WC, Dunlap WW, Allendorf FW (2000) Genetic differentiation among long-toed salamander (Ambystoma macrodactylum) populations. Copeia 2000:27–35

    Article  Google Scholar 

  • Tracy CR, Dole JW (1969) Orientation of displaced California toads, Bufo boreas, to their breeding sites. Copeia 1969:693–700

    Article  Google Scholar 

  • Waples RS, Gaggiotti O (2006) INVITED REVIEW: What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yang W, Qi Y, Bi K, Fu J (2012) Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species: a comparative transcriptomic analysis of two ranid frogs, Rana chensinensis and R. kukunoris. BMC Genom 13:588

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Tom Brekke, Kris Crandell, Sara Dykeman, Nate Muhn, Paul Scarr, and numerous field technicians who collected samples between 2008 and 2011. Sally Painter and Steve Amish provided assistance with lab work and genotyping. Marty Kardos provided assistance with randomization tests, and Eric Fuchs provided statistical advice. This manuscript was improved with comments from Mike Schwartz. This research was performed under University of Montana IACUC permit 022-09WLDBS-051209. Partial funding was provided by the Jerry O’Neal student fellowship and the U.S. Geological Survey Amphibian Research and Monitoring Initiative (ARMI). This manuscript is ARMI product number 499. Use of trade, product, or firm names does not imply endorsement by the U.S. Government.

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Correspondence to Brett R. Addis.

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Addis, B.R., Lowe, W.H., Hossack, B.R. et al. Population genetic structure and disease in montane boreal toads: more heterozygous individuals are more likely to be infected with amphibian chytrid. Conserv Genet 16, 833–844 (2015). https://doi.org/10.1007/s10592-015-0704-6

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