Abstract
Studies linking genetic structure in amphibian species with ecological characteristics have focused on large differences in dispersal capabilities. Here, we test whether two species with similar dispersal potential but subtle differences in other ecological characteristics also exhibit strong differences in genetic structure in the same landscape. We examined eight microsatellites in marbled salamanders (Ambystoma opacum) from 29 seasonal ponds and spotted salamanders (Ambystoma maculatum) from 19 seasonal ponds in a single geographic region in west-central Massachusetts. Despite overall similarity in ecological characteristics of spotted and marbled salamanders, we observed clear differences in the genetic structure of these two species. For marbled salamanders, we observed strong overall genetic differentiation (F ST = 0.091, F′ ST = 0.375), three population-level clusters of populations (K = 3), a strong pattern of isolation by distance (r = 0.58), and marked variation in family-level structure (from 1 to 23 full-sibling families per site). For spotted salamanders, overall genetic differentiation was weaker (F ST = 0.025, F′ ST = 0.102), there was no evidence of population-level clustering (K = 1), the pattern of isolation by distance (r = 0.17) was much weaker compared to marbled salamanders, and there was less variation in family-level structure (from 10 to 36 full-sibling families per site). We suspect that a combination of breeding site fidelity, effective population size, and generation interval is responsible for these marked differences. Our results suggest that marbled salamanders, compared to spotted salamanders, are more sensitive to fragmentation from various land-use activities and would be less likely to recolonize extirpated sites on an ecologically and conservation-relevant time frame.
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References
Allendorf FW, Phelps SR (1981) Use of allelic frequencies to describe population structure. Can J Fish Aquat Sci 38:1507–1514
Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program structure. Mol Ecol Resour 8:1219–1229. doi:10.1111/j.1755-0998.2008.02355.x
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Bishop SC (1941) The salamanders of New York. New York State Museum, New York
Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74:21–45
Cavalli-Sforza LL, Bodmer WF (1971) The genetics of human populations. W. H. Freeman, San Francisco
Christie MR, Marine ML, French RA, Waples RS, Blouin MS (2012) Effective size of a wild salmonid population is greatly reduced by hatchery supplementation. Heredity 109:254–260. doi:10.1038/hdy.2012.39
Cook RP (1978) Effects of acid precipitation on embryonic mortality of spotted salamanders (Ambystoma maculatum) and Jefferson salamanders (Ambystoma jeffersonianum) in the Connecticut Valley of Massachusetts. Department of Forestry and Wildlife Management, University of Massachusetts, Amherst
Croshaw DA, Schable NA, Peters MB, Glenn TC (2005) Isolation and characterization of microsatellite DNA loci from Ambystoma salamanders. Conserv Genet 6:473–479
Dawson MN, Louie KD, Barlow M, Jacobs DK, Swift CC (2002) Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California Transition Zone. Mol Ecol 11:1065–1075
Delaney KS, Riley SPD, Fisher RN (2010) A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5. doi:10.1371/journal.pone.0012767
Egan RS, Paton PWC (2004) Within-pond parameters affecting oviposition by wood frogs and spotted salamanders. Wetlands 24:1–13
Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351
Flageole S, Leclair R (1992) Demography of a salamander (Ambystoma maculatum) population studied by skeletochronology. Can J Zool 70:740–749. doi:10.1139/z92-108
Foster DR (1992) Land-use history (1730–1990) and vegetation dynamics in Central New England, USA. J Ecol 80:753–771
Gamble LR, McGarigal K, Compton BW (2007) Fidelity and dispersal in the pond-breeding amphibian, Ambystoma opacum: implications for spatio-temporal population dynamics and conservation. Biol Conserv 139:247–257. doi:10.1016/j.biocon.2007.07.001
Gamble LR, McGarigal K, Sigourney DB, Timm BC (2009) Survival and breeding frequency in marbled salamanders (Ambystoma opacum): implications for spatio-temporal population dynamics. Copeia 394–407. doi:10.1643/ch-07-241
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. doi:10.1111/j.1365-294X.2010.04673.x
Goudet J (2001) FSTAT version 2.9.3, A program to estimate and test gene diversities and fixation indices. Updated from Goudet (1995). http://www2.unil.ch/popgen/softwares/fstat.htm
Greenwald KR, Gibbs HL, Waite TA (2009) Efficacy of land-cover models in predicting isolation of marbled salamander populations in a fragmented landscape. Conserv Biol 23:1232–1241. doi:10.1111/j.1523-1739.2009.01204.x
Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin SL (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755
Husting EL (1965) Survival and breeding structure in a population of Ambystoma maculatum. Copeia 1965:352–362
Jackson SD (1990) Demography, migratory patterns and effects of pond chemistry on two syntopic mole salamanders, Ambystoma jeffersonianum and A. maculatum. Department of Forestry and Wildlife Management, University of Massachusetts, Amherst
Julian SE, King TL, Savage WK (2003a) Isolation and characterization of novel tetranucleotide microsatellite DNA markers for the spotted salamander, Ambystoma maculatum. Mol Ecol Notes 3:7–9
Julian SE, King TL, Savage WK (2003b) Novel Jefferson salamander, Ambystoma jeffersonianum, microsatellite DNA markers detect population structure and hybrid complexes. Mol Ecol Notes 3:95–97
Kaplan RH, Crump ML (1978) The non-cost of brooding in Ambystoma opacum. Copeia 1978:99–103
King RB, Lawson R (2001) Patterns of population subdivision and gene flow in three sympatric natricine snakes. Copeia 2001:602–614
Lai KJ, Gomes CP, Schwartz MK, McKelvey KS, Calkin DE, Montgomery CA (2011) The Steiner multigraph problem: wildlife corridor design for multiple species. In: Twenty-Fifth AAAI Conference on Artificial Intelligence (AAAI-11). AAAI Press, San Franciso
Lambeck RJ (1997) Focal species: a multi-species umbrella for nature conservation. Conserv Biol 11:849–856
Madison DM (1997) The emigration of radio-implanted spotted salamanders, Ambystoma maculatum. J Herpetol 31:542–551. doi:10.2307/1565607
McDonald DB, Potts WK, Fitzpatrick JW, Woolfenden GE (1999) Contrasting genetic structures in sister species of North American scrub-jays. Proc R Soc Lond B 266:1117–1125
Meirmans PG, Hedrick PW (2011) Assessing population structure: F-ST and related measures. Mol Ecol Resour 11:5–18. doi:10.1111/j.1755-0998.2010.02927.x
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. doi:10.1111/j.1471-8286.2004.00770.x
Montieth KE, Paton PWC (2006) Emigration behavior of spotted salamanders on golf courses in southern Rhode Island. J Herpetol 40:195–205. doi:10.1670/130-04a.1
Mulder CPH, Bazeley-White E, Dimitrakopoulos PG, Hector A, Scherer-Lorenzen M, Schmid B (2004) Species evenness and productivity in experimental plant communities. Oikos 107:50–63. doi:10.1111/j.0030-1299.2004.13110.x
Mullen LB, Woods AH, Schwartz MK, Sepulveda AJ, Lowe WH (2010) Scale-dependent genetic structure of the Idaho giant salamander (Dicamptodon aterrimus) in stream networks. Mol Ecol 19
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y
Neel MC, McKelvey K, Ryman N, Lloyd MW, Bull RS, Allendorf FW, Schwartz MK, Waples RS (2013) Estimation of effective population size in continuously distributed populations: there goes the neighborhood. Heredity 111:189–199. doi:10.1038/hdy.2013.37
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nicholson E, Possingham HP (2006) Objectives for multiple-species conservation planning. Conserv Biol 20:871–881. doi:10.1111/j.1523-1739.2006.00369.x
Noble GK, Brady MK (1933) Observations on the life history of the marbled salamander, Ambystoma opacum Gravenhorst. Zoologica 11:89–132
Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341
Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution, Washington DC
Petranka JW, Smith CK, Scott AF (2004) Identifying the minimal demographic unit for monitoring pond-breeding amphibians. Ecol Appl 14:1065–1078. doi:10.1890/02-5394
Plunkett EB (2009) Conservation implications of a marbled salamander, Ambystoma opacum, metapopulation model. Masters Thesis, Department of Environmental Conservation, University of Massachusetts Amherst
Pritchard K, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Purrenhage JL, Niewiarowski PH, Moore FBG (2009) Population structure of spotted salamanders (Ambystoma maculatum) in a fragmented landscape. Mol Ecol 18:235–247. doi:10.1111/j.1365-294X.2008.04024.x
R Development Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Richardson JL (2012) Divergent landscape effects on population connectivity in two co-occurring amphibian species. Mol Ecol 21:4437–4451. doi:10.1111/j.1365-294X.2012.05708.x
Rodriguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Resour. doi:10.1111/j.1755-0998.2012.03156.x Online early
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
Ryman N, Palm S, Andre C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palme A, Ruzzante DE (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045. doi:10.1111/j.1365-294X.2006.02839.x
Schwenk WS, Donovan TM (2011) A multispecies framework for landscape conservation planning. Conserv Biol 25:1010–1021. doi:10.1111/j.1523-1739.2011.01723.x
Shoop CR (1968) Migratory orientation of Ambystoma maculatum: movements near breeding ponds and displacements of migrating individuals. Biol Bull 135:230. doi:10.2307/1539630
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Sotiropoulos K, Eleftherakos K, Tsaparis D, Kasapidis P, Giokas S, Legakis A, Kotoulas G (2013) Fine scale spatial genetic structure of two syntopic newts across a network of ponds: implications for conservation. Conserv Genet 14:385–400. doi:10.1007/s10592-013-0452-4
Steele CA, Baumsteiger J, Storfer A (2009) Influence of life-history variation on the genetic structure of two sympatric salamander taxa. Mol Ecol 18:1629–1639. doi:10.1111/j.1365-294X.2009.04135.x
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 306:1783–1786. doi:10.1126/science.1103538
Tallmon DA, Gregovich D, Waples RS, Baker CS, Jackson J, Taylor BL, Archer E, Martien KK, Allendorf FW, Schwartz MK (2010) When are genetic methods useful for estimating contemporary abundance and detecting population trends? Mol Ecol Resour 10:684–692. doi:10.1111/j.1755-0998.2010.02831.x
Taylor EB (1991) A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 98:185–207
Timm BC, McGarigal K, Gamble LR (2007) Emigration timing of juvenile pond-breeding amphibians in western Massachusetts. J Herpetol 41:243–250
Turner TF, Trexler JC (1998) Ecological and historical associations of gene flow in darters (Teleostei: Percidae). Evolution 52:1781–1801
Vasconcelos HL (1999) Effects of forest disturbance on the structure of ground-foraging ant communities in central Amazonia. Biodivers Conserv 8:409–420
Vasconcelos D, Calhoun AJK (2004) Movement patterns of adult and juvenile Rana sylvatica (LeConte) and Ambystoma maculatum (Shaw) in three restored seasonal pools in Maine. J Herpetol 38:551–561. doi:10.1670/157-03a
Veysey JS, Babbitt KJ, Cooper A (2009) An experimental assessment of buffer width: implications for salamander migratory behavior. Biol Conserv 142:2227–2239. doi:10.1016/j.biocon.2009.04.024
Wang JL (2004) Sibship reconstruction from genetic data with typing errors. Genet 166:1963–1979
Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184
Waples RS (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 10:785–796. doi:10.1111/j.1755-0998.2010.02876.x
Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756
Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262. doi:10.1111/j.1752-4571.2009.00104.x
Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189:633–644. doi:10.1534/genetics.111.132233
Waples RS, Luikart G, Faulkner JR, Tallmon DA (2013) Simple life-history traits explain key effective population size ratios across diverse taxa. Proc R Soc B 280:20131339. doi:10.1098/rspb.2013.1339
Whiteley AR, Spruell P, Allendorf FW (2004) Ecological and life history characteristics predict population genetic divergence of two salmonids in the same landscape. Mol Ecol 13:3675–3688
Whiteley AR, Spruell P, Allendorf FW (2006) Can common species provide valuable information for conservation? Mol Ecol 15:2767–2786
Whiteley AR, Coombs JA, Hudy M, Robinson Z, Nislow KH, Letcher BH (2012) Sampling strategies for estimating brook trout effective population size. Conserv Genet 13:625–637. doi:10.1007/s10592-011-0313-y
Whitford WG, Vinegar A (1966) Homing, survivorship, and overwintering of larvae of spotted salamanders, Ambystoma maculatum. Copeia 1966:515–519
Whitlock MC, McCauley DE (1999) Indirect measures of gene flow and migration: FST does not equal 1/(4Nm + 1). Heredity 82:117–125. doi:10.1038/sj.hdy.6884960
Wright S (1969) Evolution and the genetics of populations. vol 2. The Theory of Gene Frequencies. University of Chicago Press, Chicago
Zamudio KR, Wieczorek AM (2007) Fine-scale spatial genetic structure and dispersal among spotted salamander (Ambystoma maculatum) breeding populations. Mol Ecol 16:257–274. doi:10.1111/j.1365-294X.2006.03139.x
Acknowledgments
We thank B. Compton for spotted salamander sample collection and helpful discussions. M. Chesser and J. Estes helped with sample collection. J. Estes, S. Jane, A. Pant, and K. Pilgrim conducted genetic data collection. S. Jackson, B. Cook, and P. Fenton provided important natural history information. We thank D. Chapple and two anonymous reviewers for helpful comments on an earlier draft of this manuscript.
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Whiteley, A.R., McGarigal, K. & Schwartz, M.K. Pronounced differences in genetic structure despite overall ecological similarity for two Ambystoma salamanders in the same landscape. Conserv Genet 15, 573–591 (2014). https://doi.org/10.1007/s10592-014-0562-7
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DOI: https://doi.org/10.1007/s10592-014-0562-7