Abstract
Habitat fragmentation and degradation associated with suburbanization can have negative consequences on population persistence through the reduction of dispersal and concomitant gene flow. Using eight polymorphic microsatellite loci, we assessed the effects of forest fragmentation, water quality and hydroperiod on the genetic structure of a vernal pool-breeding amphibian, the wood frog (Lithobates sylvaticus), across 20 ponds in an unfragmented, forested landscape and 45 ponds in a landscape fragmented by moderate suburban development. Analyses were performed at the broad scale of the study area and at a fine scale, with spatially independent clusters of ponds selected within each landscape. Bayesian clustering approaches and AMOVA identified little population structure at the scale of the study area. At the fine scale, genetic structure was correlated with geographic distance and the presence of roads in two of the three fragmented clusters. Spatial autocorrelation analyses detected positive spatial genetic structure and restricted dispersal in one of the clusters in the fragmented landscape. We identified barriers associated with roads and suburban development in the fragmented landscape and with large bodies of water and elevation in the unfragmented landscape. Lastly, we found no biologically meaningful effects of water quality or hydroperiod on genetic variation. The results of this study indicate that wood frog populations are well connected, with high gene flow, across the landscape of southeastern New Hampshire, and that fragmenting features of suburbanization to date have a small but detectable impact on fine-scale genetic structure. The potential exists for greater impacts with higher levels of development or longer time scales. Our findings also highlight the importance of replication in landscape genetic studies, as the genetic response we detected varied with a gradient of fragmentation.



References
Adriaensen F, Chardon JP, De Blust G, Swinnen E, Villalba S, Gulinck H, Matthysen E (2003) The application of ‘least-cost’ modeling as a functional landscape model. Landscape Urban Plan 64:233–247
Alcaide M, Serrano D, Negro JJ, Tella JL, Laaksonen T, Müller C, Gal A, Korpimäki A (2009) Population fragmentation leads to isolation by distance but not genetic impoverishment in the philopatric Lesser Kestrel: a comparison with the widespread and sympatric Eurasian Kestrel. Heredity 102:190–198
Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annu Rev Ecol Syst 30:133–165
Anderson CD, Epperson BK, Fortin M-J, Holderegger R, James PMA, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575
Andrén H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366
Babbitt KJ, Baber MJ, Tarr TL (2003) Patterns of larval amphibian distribution along a wetland hydroperiod gradient. Can J Zool 81:1539–1552
Babbitt KJ, Baber MJ, Brandt LA (2006) The effects of woodland proximity and wetland characteristics on wetland larval anuran assemblages. Can J Zool 84:510–519
Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164
Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, Holderegger R, Wagner HH et al (2009a) Identifying future research needs in landscape genetics: where to from here? Landscape Ecol 24:455–463
Balkenhol N, Waits LP, Dezzani RJ (2009b) Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data. Ecography 32:818–830
Berven KA, Grudzien TA (1990) Dispersal in the wood frog (Ranasylvatica): implications for genetic populationstructure. Evolution 44:2047–2056
Brede EG, Beebee TJC (2004) Contrasting population structures in two sympatric anurans: implications for species conservation. Heredity 92:111–117
Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol S40:193–216
Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Cavalli-Sforza, L.L. and Edwards, A.W.F. 1967. Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Clark RW, Brown WS, Stechert R, Zamudio KR (2010) Roads, interrupted dispersal, and genetic diversity in timber rattle snake. Conserv Biol 4:1059–1069
Collins SJ, Russell RW (2009) Toxicity of road salt to Nova Scotia amphibians. Environ Pollut 157:320–324
Compton BW, McGarigal K, Cushman SA, Gamble LR (2007) A resistant kernel model of connectivity for amphibians that breed in vernal pools. Conserv Biol 21:788–799
Crosby MKA, Licht LE, Fu J (2009) The effect of habitat fragmentation on fine scale population structure of wood frogs (Ranasylvatica). Conserv Genet 10:1707–1718
Crouch WB, Paton PWC (2000) Using egg-mass counts to monitor wood frog populations. Wildlife Soc B 28:895–901
Cushman SA (2006) Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 128:31–240
De-Lucas AI, González-Martínez SC, Vendramin GG, Hidalgo E, Heuertz M (2009) Spatial genetic structure in continuous and fragmented populations of Pinuspinaster Aiton. Mol Ecol 18:4564–4576
Dodd CK, Barichivich WJ, Smith LL (2004) Effectiveness of a barrier wall and culverts in reducing wildlife mortality on a heavily traveled highway in Florida. Biol Conserv 83:43–54
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
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515
Foll M, Gaggiotti O (2006) Identifying the environmental factors that determine the genetic structure of populations. Genetics 174:875–891
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, New York
Funk WC, Blouin MS, Corn PS, Maxell BA, Pilliod DS, Amish S, Allendorf SW (2005) Population structure of Columbia spotted frogs (Ranaluteiventris) is strongly affected by the landscape. Mol Ecol 14:483–496
Gaggiotti OE, Foll M (2010) Quantifying population structure using the F-model. Mol Ecol Resour 10:821–830
Gallant AL, Klaver RW, Casper GS, Lannoo MJ (2007) Global rates of habitat loss and implications for amphibian conservation. Copeia 2007:967–979
Giordano AR, Ridenhour BJ, Storfer A (2007) The influence of altitude and topography on genetic structure in the long-toed salamander (Ambystoama macrodactylum). Mol Ecol 16:1625–1637
Goldberg CS, Waits LP (2010) Comparative landscape genetics of two pond-breeding amphibian species in a highly modified agricultural landscape. Mol Ecol 19:3650–3663
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Guerry AD, Hunter ML (2002) Amphibian distributions in a landscape of forests and agriculture: an examination of landscape composition and configuration. Conserv Biol 16:745–754
Hanski I, Gilpin ME (1997) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San Diego
Hardy OJ, Vekemans S (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hardy OJ, Maggia L, Bandou L, Breyne E, Breyne P, Caron H, Chevallier MH, Doligez A, Dutech C, Kremer A, Latouche-Hallé C, Troispoux V, Veron V, Degen B (2006) Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Mol Ecol 15:559–571
Herrmann HL, Babbitt KJ, Baber MJ, Congalton RJ (2005) Effects of landscape characteristics on amphibian distribution in a forest-dominated landscape. Biol Conserv 123:139–149
Hitchings SP, Beebee TJC (1997) Genetic substructuring as a result of barriers to gene flow in urban Ranatemporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127
Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207
Holzhauer SIJ, Ekschmitt K, Sander AC, Dauber J, Wolters V (2006) Effect of historic landscape change on the genetic structure of the bush-cricket Metriopteraroeseli. Landscape Ecol 21:891–899
Horne MT, Dunson WA (1994) Interactive effects of low pH, toxic metals, and DOC on a simulated temporary pond community. Environ Pollut 89:155–161
Horne MT, Dunson WA (1995) Effects of low pH, metals, and water hardness on larval amphibians. Arch Environ Contam Toxicol 29:500–505
Howard RD, Kluge AG (1985) Proximate mechanisms of sexual selection in wood Frogs. Evolution 39:260–277
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol 9:1322–1332
Hunt A, Dickens HJ, Whelan RJ (1987) Movement of mammals through tunnels under railway lines. Aust J Zool 24:89–93
Jackson SD, Griffin CR (2000) A strategy for mitigating highway impacts on wildlife. In: Messmer TA, West B (eds) Wildlife and highways: seeking solutions to an ecological and socio-economic dilemma. The Wildlife Society, Bethesda, pp 143–159
Julian SE, King TL (2003) Novel tetranucleotide microsatellite DNA markers for the wood frog, Ranasylvatica. Mol Ecol Notes 3:256–258
Jump AS, Peñuelas J (2006) Genetic effects of chronic habitat fragmentation in a wind pollinated tree. Proc Natl Acad Sci USA 103:8096–8100
Karraker NE, Gibbs JP, Vonesh JR (2008) Impacts of road deicing salt on the demography of vernal pool-breeding amphibians. Ecol Appl 18:724–734
Keller I, Nentwig W, Largiader CR (2004) Recent habitat fragmentation due to roads can lead to significant genetic differentiation in an abundant flightless ground beetle. Mol Ecol 13:2983–2994
Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064
Keyghobadi N, Roland J, Matter SF, Strobeck C (2005) Among- and within-patch components of genetic diversity respond at different rates to habitat fragmentation: an empirical demonstration. Proc R Soc B Biol Sci 272:553–560
Lada, H, Thomson JR, Mac Nally R, Taylor AC (2008) Impacts of massive landscape change on a carnivorous marsupial in south-eastern Australia: inferences from landscape genetics analysis. J Appl Ecol 45:1732–1741
Lampert KP, Rand AS, Mueller UG, Ryan MJ (2003) Fine-scale genetic pattern and evidence for sex-biased dispersal in the tungara frog, Physalaemuspustulosus. Mol Ecol 12:3325–3334
Landguth EL, Cushman SA, Schwartz MK, McKelvey KS, Murphy M, Luikarts G (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191
Lesbarres RES, Lode DT, Merila J (2004) What type of underpass could potentially reduce amphibian road kills. Oryx 38:1–5
Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull Entomol Soc Am 15:237–240
Lewis PO, Zaykin D (2001) Genetic Data Analysis: computer program for the analysis of allelic data, Version 1.0 (d16c). Available from http://lewis.eeb.uconn.edu/lewishome/software.html
Lindenmayer D, Hobbs RJ, Montague-Drake R, Alexandra J, Bennett A, Burgman M, Cale P, Calhoun A, Cramer V, Cullen P, Driscoll D, Fahrig L, Fischer J, Franklin J, Haila Y, Hunter M, Gibbons P, Lake S, Luck G, MacGregor C, McIntyre S, Mac Nally R, Manning A, Miller J, Mooney H, Noss R, Possingham H, Saunders D, Schmiegelow F, Scott M, Simberloff D, Sisk T, Tabor G, Walker B, Wiens J, Woinarski J, Zavaleta E (2008) A checklist for ecological management of landscapes for conservation. Ecol Lett 11:78–91
Manni F, Guerard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by “Monmonier’s algorithm”. Hum Biol 76:173–190
Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49
Morin PA, Manaster C, Mesnick SL, Holland R (2009) Normalization and binning of historical and multi-source microsatellite data: overcoming the problems of allele size shift with ALLELOGRAM. Mol Ecol Resour 9:1451–1455
Murphy M, Evans J, Cushman S, Storfer A (2008) Representing genetic variation as continuous surfaces: an approach for identifying spatial dependency in landscape genetic studies. Ecography 31:685–697
Murphy M, Evans J, Storfer A (2010a) Quantify ecological process at multiple spatial scales using landscape genetics: Bufoboreas connectivity in Yellowstone National Park. Ecology 91:252–261
Murphy M, Dezzani R, Pilliod D, Storfer A (2010b) Landscape genetics of high mountain frog metapopulations. Mol Ecol 19:3634–3649
Newman RA, Squire T (2001) Microsatellite variation and fine-scale population structure in the wood frog (Ranasylvatica). Mol Ecol 10:1087–1100
Oksanen J, Kindt R, Legendre P, O’Hara RB (2006) VEGAN: community ecology package, R package ver. 1.8–3. Available from http://cran.r-project.org/
Pannell JR, Charlesworth B (1999) Neutral genetic diversity in a metapopulation with recurrent local extinction and recolonization. Evolution 53:664–676
Patrick DA, Schalk CM, Gibbs JP, Woltz HW (2010) Effective culvert placement and design to facilitate passage of amphibians across roads. J Herpetol 44:618–626
Peakall R, Smouse PE (1995) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat Rattusfuscipes. Evolution 57:1182–1195
Pechmann JHK, Scott DE, Gibbons JW, Semlitsch RD. 1989. Influence of wetland hydroperiod on diversity and abundance of metamorphosing juvenile amphibians. Wetl Ecol Manag 1:3–11
Pough FH, Wilson RE (1977) Acid precipitation and reproductive success of Ambystoma salamanders. Water Air Soil Poll 7:531–544
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Richter KO, Azous AL (1995) Amphibian occurrence and wetland characteristics in the Puget Sound Basin. Wetlands 15:306–312
Riley SPD, Pollinger JP, Sauvajot RM, York EC, Bromley C, Fuller TK, Wayne RK (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741
Rothermal BB (2004) Migratory success of juveniles: a potential constraint on connectivity for pond-breeding amphibians. Ecol Appl 14:1535–1546
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Rowe G, Beebee TJC, Burke T (2000) A microsatellite analysis of natterjack toad, Bufocalamita, metapopulations. Oikos 88:641–651
Sadinski WJ, Dunson WA (1992) A multilevel study of effects of low pH on amphibians of temporary ponds. J Herpetol 26:413–422
Sanzo D, Hecnar SJ (2006) Effects of deicing salt (NaCl) on larval wood frogs (Ranasylvatica). Environ Pollut 140:247–256
Semlitsch RD, Reyer HU (1992) Performance of tadpoles from the hybridogeneticRanaesculenta complex: interactions with pond drying and interspecific competition. Evolution 46:665–676
Seppä P, Laurila A (1999) Genetic structure of island populations of the anurans Ranatemporaria and Bufobufo. Heredity 82:309–317
Shepard DB, Kuhns AR, Dreslik MJ, Phillips CA (2008) Roads as barriers to animal movement in fragmented landscapes. Anim Conserv 11:288–296
Short Bull RA, Cushman SA, Mace R, Chilton T, Kendall KC, Landguth EL, Schwartz MK, McKelvey K, Allendorf FW, Luikart G (2011) Why replication is important in landscape genetics: American black bear in the Rocky Mountains. Mol Ecol 20:1092–1107
Sinsch U (1990) Migration and orientation in anuran amphibians. Ethol Ecol Evol 2:65–79
Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Smouse PE, Peakall R, Gonzalez E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17:3389–3400
Snodgrass JW, Casey RE, Joseph DE, Simon JA (2008) Microcosm investigations of storm water pond sediment toxicity to embryonic and larval amphibians: variation in sensitivity among species. Environ Pollut 154:291–297
Society for the Protection of New Hampshire’s Forest (SPNHF) (2005) New Hampshire’s changing landscape. SPNHF, Concord
Spear SF, Peterson CR, Matocq MD, Storfer A (2005) Landscapegenetics of the blotched tiger salamander (Ambystomatigrinum melanostictum). Mol Ecol 14:2553–2564
Squire T, Newman RA (2002) Fine-scale population structure in the wood frog (Ranasylvatica) in a northern woodland. Herpetologica 58:119–130
Stevens CE, Paszkowski CA (2004) Using chorus-size ranks from call surveys to estimate reproductive activity of the wood frog (Ranasylvatica). J Herpetol 38:404–410
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP (2010) Landscape genetics: where are we now? Mol Ecol 19:3496–3514
Thorne S, Sundquist D (2001) New Hampshire’s vanishing forest: conversion, fragmentation, and parcelization of forest in the granite state. Society for the Protection of New Hampshire Forest, Concord
Trombulak SC, Frissell CA (2000) Review of ecological effects of roads on terrestrial and aquatic communties. Conserv Biol 14:18–30
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
Vandergast AG, Perry WM, Lugo RV, Hathaway SA (2010) Genetic landscapes GIS Toolbox: tools to map patterns of genetic divergence and diversity. Mol Ecol Resour 11:158–161
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935
Veysey JS, Mattfeldt SD, Babbitt KJ (2011) Comparative influence of isolation, landscape, and wetland characteristics on egg-mass abundance of two pool-breeding amphibian species. Landscape Ecol 26:661–672
Vos CC, Antonisse-de Jong AG, Goedhart PW, Smulders MJM (2001) Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Ranaarvalis). Heredity 86:598–608
Wade MJ, McCauley DE (1988) Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42:995–1005
Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
Woltz HW, Gibbs JP, Ducey PK (2008) Road crossing structures for amphibians and reptiles: informing design through behavioral analysis. Biol Conserv 141:2745–2750
Wright S (1943) Isolation by distance. Genetics 28:114–138
Yanes MJ, Velasco M, Suarez F (1995) Permeability of roads and railways to vertebrates: the importance of culverts. Biol Conserv 71:217–222
Acknowledgments
Partial funding for this research was provided by the New Hampshire Agricultural Experiment Station. This is Scientific Contribution Number 2512. We are grateful to S. Coster, J. Purrenhage, and J. Walsh for their assistance in the field and to numerous private landowners for allowing us access to ponds on their properties. We thank the University of New Hampshire Hubbard Center for Genome Studies and J. Anderson for assistance with fragment analysis, and D. Berlinsky for generous use of his laboratory facilities. We also thank M. Daley, J. Potter, and the UNH Water Quality Analysis Laboratory for assistance with water quality analyses and D. Hocking for statistical advice.
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Gabrielsen, C.G., Kovach, A.I., Babbitt, K.J. et al. Limited effects of suburbanization on the genetic structure of an abundant vernal pool-breeding amphibian. Conserv Genet 14, 1083–1097 (2013). https://doi.org/10.1007/s10592-013-0497-4
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DOI: https://doi.org/10.1007/s10592-013-0497-4