Differential dispersal shapes population structure and patterns of genetic differentiation in two sympatric pond breeding salamanders

Conservation Genetics

Volumn 16, Issue 1, 2015, Pages 59-69

  Peterman, William E ^a,b   Anderson, Thomas L ^a   Ousterhout, Brittany H ^a   Drake, Dana L ^a   Semlitsch, Raymond D ^a   Eggert, Lori S ^a  

^a Division of Biological Sciences   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Ambystoma annulatum; Ambystoma maculatum; Amphibian; Landscape genetics; Life history; Military installation; Ozark

Indexed keywords

EID: 84939885689     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-014-0640-x     Document Type: Article

References (67)

1. Adamack AT, Gruber B (2014) PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol Evol 5:384–387
2. Anderson TA, Hocking DJ, Conner CA, Earl JE, Harper EB, Osbourn MJ, Peterman WE, Rittenhouse TAG, Semlitsch RD (in review) The influence of priority effects on metamorph traits and recruitment of two pond-breeding salamanders
3. Bates DM, Maechler M, Bolker BM, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-6. http://CRAN.R-project.org/package=lme4
4. Beerli P (2004) Effect of unsampled populations on the estimation of population sizes and migration rates between sampled populations. Mol Ecol 13:827–836
5. Brede E, Beebee T (2004) Contrasting population structures in two sympatric anurans: implications for species conservation. Heredity 92:110–117
6. Brussock PP III, Brown AV (1982) Selection of breeding ponds by the ringed salamander, Ambystoma annulatum. Proc Ark Acad Sci 36:82–83
7. Caro TM (2003) Umbrella species: critique and lessons from East Africa. Anim Conserv 6:171–181
8. Clarke RT, Rothery P, Raybould AF (2002) Confidence limits for regression relationships between distance matrices: estimating gene flow with distance. JABES 7:361–372
9. Corander J, Marttinen P (2006) Bayesian identification of admixture events using multilocus molecular markers. Mol Ecol 15:2833–2843
10. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374
11. Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Statistics 23:111–129
12. Ficetola GF, Sacchi R, Scali S, Gentilli A, De Bernardi F, Galeotti P (2007) Vertebrates respond differently to human disturbance: implications for the use of a focal species approach. Acta Oecol 31:109–118
13. Gaggiotti OE, Foll M (2010) Quantifying population structure using the F-model. Mol Ecol Resour 10:821–830
14. 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
15. 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
16. Hanski I, Gilpin M (1997) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San Diego
17. Hocking DJ, Rittenhouse TAG, Rothermel BB, Johnson BR, Conner CA, Harper EB, Semlitsch RD (2008) Breeding and recruitment phenology of amphibians in Missouri oak-hickory forests. Am Midl Nat 160:41–60
18. Jacobson RB, Primm AT (1997) Historical land-use changes and potential effects on stream disturbance in the Ozark Plateaus, Missouri. United States Geological Survey Water-Supply Paper 2484
19. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555
20. Koen EL, Bowman J, Garroway CJ, Wilson PJ (2013) The sensitivity of genetic connectivity measures to unsampled and under-sampled sites. PLoS One 8:e56204
21. Lannoo MJ (ed) (2005) Amphibian Declines: the Conservation Status of United States Species. University of California Press, Berkeley
22. Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051
23. 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
24. McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561
25. Meirmans PG, Hedrick PW (2011) Assessing population structure: FST and related measures. Mol Ecol Resour 11:5–18
26. 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
27. Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145
28. Naujokaitis-Lewis IR, Rico Y, Lovell J, Fortin M-J, Murphy MA (2012) Implications of incomplete networks on estimation of landscape genetic connectivity. Conserv Genet 14:287–298
29. Nicholson E, Possingham HP (2006) Objectives for Multiple-Species Conservation Planning. Conserv Biol 20:871–881
30. Olsen JB, Crane PA, Flannery BG, Dunmall K, Templin WD, Wenburg JK (2011) Comparative landscape genetic analysis of three Pacific salmon species from subarctic North America. Conserv Genet 12:223–241
31. Peterman WE, Semlitsch RD (2013) Fine-scale habitat associations of a terrestrial salamander: the role of environmental gradients and implications for population dynamics. PLoS One 8:e62184
32. Peterman WE, Connette GM, Spatola BN, Eggert LS, Semlitsch RD (2012) Identification of polymorphic loci in Ambystoma annulatum and review of cross-species microsatellite use in the genus Ambystoma. Copeia 2012:570–577
33. Peterman WE, Brocato ER, Pauley LR, Stuart EC, Semlitsch RD, Eggert LS (2013a) Development and characterization of 18 microsatellite loci for the spotted salamander (Ambystoma maculatum) using paired-end Illumina shotgun sequencing. Conserv Genet Resour 5:989–991
34. Peterman WE, Pauley LR, Brocato ER, Stuart EC, Semlitsch RD, Eggert LS (2013b) Development and characterization of 22 microsatellite loci for the ringed salamander (Ambystoma annulatum) using paired-end Illumina shotgun sequencing. Conserv Genet Resour 5:993–995
35. Peterman WE (2014) ResistanceGA: an R package for the optimization of resistance surfaces using genetic algorithms. R Package version 2.0-3. https://github.com/wpeterman/ResistanceGA
36. Peterman WE, Anderson TL, Drake DL, Ousterhout BH, Semlitsch RD (2014a) Maximizing pond biodiversity across the landscape: a case study of larval ambystomatid salamanders. Anim Conserv 17:275–285
37. Peterman WE, Connette GM, Semlitsch RD, Eggert LS (2014b) Ecological resistance surfaces predict fine-scale genetic differentiation in a terrestrial woodland salamander. Mol Ecol 23:2402–2413
38. Petranka JW (1998) Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC
39. Pflüger FJ, Balkenhol N (2014) A plea for simultaneously considering matrix quality and local environmental conditions when analyzing landscape impacts on effective dispersal. Mol Ecol. doi:10.1111/mec.12712
40. Phillips CA, Suau G, Templeton AR (2000) Effects of holocene climate fluctuation on mitochondrial DNA variation in the ringed salamander, Ambystoma annulatum. Copeia 2000:542–545
41. Pierce KB, Lookingbill T, Urban D (2005) A simple method for estimating potential relative radiation (PRR) for landscape-scale vegetation analysis. Landsc Ecol 20:137–147
42. Pittman SE, Semlitsch RD (2013) Habitat type and distance to edge affect movement behavior of juvenile pond-breeding salamanders. J Zool 291:154–162
43. Pittman SE, Osbourn MS, Semlitsch RD (2014) Movement ecology of amphibians: a missing component for understanding population declines. Biol Conserv 169:44–53
44. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
45. Purrenhage JL, Niewiarowski PH, Moore FB-G (2009) Population structure of spotted salamanders (Ambystomamaculatum) in a fragmented landscape. Mol Ecol 18:235–247
46. Raymond M, Rousset F (1995) GenePop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
47. R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
48. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
49. Richardson JL (2012) Divergent landscape effects on population connectivity in two co-occurring amphibian species. Mol Ecol 21:4437–4451
50. 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
51. Rothermel BB, Semlitsch RD (2006) Consequences of forest fragmentation for juvenile survival in spotted (Ambystoma maculatum) and marbled (Ambystoma opacum) salamanders. Can J Zool 84:797–807
52. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
53. Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452
54. Schwenk WS, Donovan TM (2011) A multispecies framework for landscape conservation planning. Conserv Biol 25:1010–1021
55. Semlitsch RD, Anderson TL, Osbourn MS, Ousterhout BH (2014) Structure and dynamics of ringed salamander (Ambystoma annulatum) populations in Missouri. Herpetologica 70:14–22
56. Shulse CD, Semlitsch RD, Trauth KM, Williams AD (2010) Influences of design and landscape placement parameters on amphibian abundance in constructed wetlands. Wetlands 30:915–928
57. Slatkin M (2005) Seeing ghosts: the effect of unsampled populations on migration rates estimated for sampled populations. Mol Ecol 14:67–73
58. Smith MA, Green DM (2005) Dispersal and the metapopulation paradigm in amphibian ecology and conservation: are all amphibian populations metapopulations? Ecography 28:110–128
59. 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
60. Spear SF, Storfer A (2008) Landscape genetic structure of coastal tailed frogs (Ascaphus truei) in protected vs. managed forests. Mol Ecol 17:4642–4656
61. 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
62. Trenham PC, Koenig WD, Mossman MJ, Stark SL, Jagger LA (2003) Regional dynamics of wetland-breeding frogs and toads: turnover and synchrony. Ecol Appl 13:1522–1532
63. Van Buskirk J (2012) Permeability of the landscape matrix between amphibian breeding sites. Ecol Evol 2:3160–3167
64. 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
65. Whiteley A, McGarigal K, Schwartz M (2014) Pronounced differences in genetic structure despite overall ecological similarity for two Ambystoma salamanders in the same landscape. Conserv Genet. doi:10.1007/s10592-10014-10562-10597
66. Zamudio KR, Savage WK (2003) Historical isolation, range expansion, and secondary contact of two highly divergent mitochondrial lineages in spotted salamanders (Ambystoma maculatum). Evolution 57:1631–1652
67. Zamudio KR, Wieczorek AM (2007) Fine-scale spatial genetic structure and dispersal among spotted salamander (Ambystoma maculatum) breeding populations. Mol Ecol 16:257–274