Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis

Molecular Ecology

Volumn 20, Issue 8, 2011, Pages 1582-1600

  Richter Boix, Alex ^a   Quintela, María ^a,b   Segelbacher, Gernot ^a,c   Laurila, Anssi ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UNIVERSITY OF A CORUÑA   (Spain)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

conservation units; directional selection; habitat heterogeneity; local adaptation; population structure; stabilizing selection

Indexed keywords

FRESH WATER; MICROSATELLITE DNA;

ADAPTATION; ALLELE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; ECOSYSTEM; FROG; GENE FLOW; GENE FREQUENCY; GENE REGULATORY NETWORK; GENETIC SELECTION; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; POPULATION GENETICS; SWEDEN;

ADAPTATION, BIOLOGICAL; ALLELES; ANIMALS; ECOSYSTEM; FRESH WATER; GENE FLOW; GENE FREQUENCY; GENE REGULATORY NETWORKS; GENETIC VARIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; RANIDAE; SELECTION, GENETIC; SWEDEN;

AMPHIBIA; RANA ARVALIS;

EID: 79953788317     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2011.05025.x     Document Type: Article

References (112)

1. Angers B, Bernatchez L, (1997) Complex evolution of a salmonid microsatellite locus and its consequences in inferring allelic divergence from size information. Molecular Biology and Evolution, 14, 230-238. (Pubitemid 27102669)
2. Antao T, Lopes A, Lopes R, Beja-Pereira A, Luikart G, (2008) LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics, 9, 323.
3. Arens P, van der Sluis T, van't Westende W, et al. (2007) Genetic population differentiation and connectivity among fragmented Moor frog (Rana arvalis) populations in The Netherlands. Landscape Ecology, 22, 1489-1500. (Pubitemid 350059880)
4. Beaumont MA, Balding DJ, (2004) Identifying adaptive genetic divergence among populations from genome scans. Molecular Ecology, 13, 969-980. (Pubitemid 38390600)
5. Beaumont M, Nichols R, (1996) Evaluating loci for use in the genetic analysis of population structure. Proceedings: Biological Sciences, 263, 1619-1626. (Pubitemid 27055553)
6. Bekessy SA, Ennos RA, Burgman MA, Newton AC, Ades PK, (2003) Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biological Conservation, 110, 267-275. (Pubitemid 36174787)
7. 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). Molecular Biology and Evolution, 23, 773-783.
8. Brede EG, Beebee TJC, (2003) Contrasting population structures in two sympatric anurans: implications for species conservation. Heredity, 92, 110-117.
9. Callen DF, Thompson AD, Shen Y, et al. (1993) Incidence and origin of "null" alleles in the (AC)n microsatellite markers. American Journal of Human Genetics, 52, 922-927. (Pubitemid 23313713)
10. Chan LM, Zamudio KR, (2009) Population differentiation of temperate amphibians in unpredictable environments. Molecular Ecology, 18, 3185-3200.
11. Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC, (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Molecular Ecology, 18, 2746-2765.
12. Chapuis MP, Estoup A, (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24, 621-631. (Pubitemid 46355787)
13. Chen C, Durand E, Forbes F, François O, (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes, 7, 747-756. (Pubitemid 47329398)
14. Chessel D, Dufour AB, Thioulouse J, (2004) The ade4 package-I: One-table methods. R News, 4, 5-10.
15. Cornuet JM, Luikart G, (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics, 144, 2001-2014. (Pubitemid 26427944)
16. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK, (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution, 15, 290-295. (Pubitemid 30409541)
17. Crawford NG, (2010) SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources, 10, 556-557.
18. Dakin EE, Avise JC, (2004) Microsatellite null alleles in parentage analysis. Heredity, 93, 504-509. (Pubitemid 39415597)
19. Dyer RJ, (2009) GeneticStudio: a suite of programs for spatial analysis of genetic-marker data. Molecular Ecology Resources, 9, 110-113.
20. Dyer RJ, Nason JD, (2004) Population Graphs: the graph theoretic shape of genetic structure. Molecular Ecology, 13, 1713-1727. (Pubitemid 38847581)
21. Dyer RJ, Nason JD, Garrick RC, (2010) Landscape modelling of gene flow: improved power using conditional genetic distance derived from the topology of population networks. Molecular Ecology, 19, 3746-3759.
22. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity, 103, 285-298.
23. Fernández J, Toro MA, Caballero A, (2008) Management of subdivided populations in conservation programs: cevelopment of a novel dynamic system. Genetics, 179, 683-692.
24. Ferrière R, Dieckmann U, Couvet D, (2004) Evolutionary Conservation Biology. Cambridge University Press, New York.
25. Ficetola GF, Garner TWJ, Bernardi FD, (2007) Genetic diversity, but not hatching success, is jointly affected by postglacial colonization and isolation in the threatened frog, Rana latastei. Molecular Ecology, 16, 1787-1797. (Pubitemid 46639970)
26. Foll M, Gaggiotti O, (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics, 180, 977-993.
27. Fortuna MA, Gõmez-Rodríguez C, Bascompte J, (2006) Spatial network structure and amphibian persistence in stochastic environments. Proceedings of the Royal Society B: Biological Sciences, 273, 1429-1434. (Pubitemid 47308765)
28. Frankham R, Ballou JD, Briscoe DA, (2002) Introduction to Conservation Genetics. Cambridge University Press, Cambridge.
29. Funk WC, Blouin MS, Corn PS, et al. (2005) Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Molecular Ecology, 14, 483-496. (Pubitemid 40210677)
30. Garner T, Tomio G, (2001) Microsatellites for use in studies of the Italian Agile Frog, Rana latastei (Boulenger). Conservation Genetics, 2, 77-80. (Pubitemid 33638244)
31. Garroway CJ, Bowman J, Carr D, Wilson PJ, (2008) Applications of graph theory to landscape genetics. Evolutionary Applications, 1, 620-630.
32. Gebremedhin B, Ficetola GF, Naderi S, et al. (2009) Combining genetic and ecological data to assess the conservation status of the endangered Ethiopian walia ibex. Animal Conservation, 12, 89-100.
33. Gibbs JP, (2000) Wetland loss and biodiversity conservation. Conservation Biology, 14, 314-317. (Pubitemid 30187768)
34. Giordano AR, Benjamin JR, Storfer A, (2007) The influence of altitude and topography on genetic structure in the long-toed salamander (Ambystoma macrodactulym). Molecular Ecology, 16, 1625-1637. (Pubitemid 46525385)
35. Gomulkiewicz R, Holt RD, Barfield M, (1999) The effects of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theoretical Population Biology, 55, 283-296. (Pubitemid 29384459)
36. Grimaldi M-C, Crouau-Roy B, (1997) Microsatellite allelic homoplasy due to variable flanking sequences. Journal of Molecular Evolution, 44, 336-340. (Pubitemid 27098372)
37. Hecnar SJ, M'Closkey RT, (1996) Regional dynamics and the status of amphibians. Ecology, 77, 2091-2097.
38. Helbing CC, Werry K, Crump D, et al. (2003) Expression profiles of novel thyroid hormone-responsive genes and proteins in the tail of Xenopus laevis tadpoles undergoing precocious metamorphosis. Molecular Endocrinology, 17, 1395-1409. (Pubitemid 36819959)
39. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V, (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity, 99, 592-600. (Pubitemid 350146926)
40. Hermisson J, (2009) Who believes in whole-genome scans for selection? Heredity, 103, 283-284.
41. Hoffmann AA, Willi Y, (2008) Detecting genetic responses to environmental change. Nature Reviews Genetics, 9, 421-432. (Pubitemid 351693974)
42. Hoffmann AA, Hallas RJ, Dean JA, Schiffer M, (2003) Low potential for climatic stress adaptation in a rainforest Drosophila species. Science, 301, 100-102. (Pubitemid 36801570)
43. Höglund J, (2009) Evolutionary Conservation Genetics. Oxford University Press, Oxford.
44. ST. Nature Reviews Genetics, 10, 639-650.
45. Jehle R, Burke T, Arntzen JW, (2005) Delineating fine-scale genetic units in amphibians: probing the primacy of ponds. Conservation Genetics, 6, 227-234. (Pubitemid 40747865)
46. Joost S, Bonin A, Bruford MW, et al. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969. (Pubitemid 47397327)
47. ST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
48. Kane NC, Rieseberg LH, (2007) Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics, 175, 1823-1834. (Pubitemid 46789966)
49. Kinnison MT, Hairston NG, (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Functional Ecology, 21, 444-454. (Pubitemid 46802145)
50. Kohn MH, Murphy WJ, Ostrander EA, Wayne RK, (2006) Genomics and conservation genetics. Trends in Ecology & Evolution, 21, 629-637. (Pubitemid 44528810)
51. Koskinen MT, Haugen TO, Primmer CR, (2002) Contemporary fisherian life-history evolution in small salmonid populations. Nature, 419, 826-830. (Pubitemid 35238566)
52. Lande R, (1988) Genetics and demography in biological conservation. Science, 241, 1455-1460. (Pubitemid 19321337)
53. Legendre P, Legendre L, (1998) Numerical Ecology, 2nd edn. Elsevier, Amsterdam.
54. Lehmann T, Hawley WA, Collins FH, (1996) An evaluation of evolutionary constraints on microsatellite loci using null alleles. Genetics, 144, 1155-1163. (Pubitemid 26378257)
55. Lenormand T, (2002) Gene flow and the limits to natural selection. Trends in Ecology & Evolution, 17, 183-189. (Pubitemid 34219312)
56. Lowry DB, (2010) Landscape evolutionary genomics. Biology Letters, 6, 502-504.
57. Luikart G, Pilgrim K, Visty J, Ezenwa VO, Schwartz MK, (2008) Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep. Biology Letters, 4, 228-231. (Pubitemid 351346302)
58. Lynch M, (1996) A quantitative genetic perspective on conservation issues. In: Conservation Genetics: Case Histories from Nature (eds, Avise JC, Hamrick JL,), pp. 471-501. Chapman and Hall, New York.
59. McCaffery RM, Maxell BA, (2010) Decreased winter severity increases viability of a montane frog population. Proceedings of the National Academy of Sciences, 107, 8644-8649.
60. McKay JK, Latta RG, (2002) Adaptive population divergence: markers, QTL and traits. Trends in Ecology & Evolution, 17, 285-291. (Pubitemid 34518298)
61. McMenamin SK, Hadly EA, Wright CK, (2008) Climatic change and wetland desiccation cause amphibian decline in Yellowstone National Park. Proceedings of the National Academy of Sciences USA, 105, 16988-16993.
62. Meglecz E, Petenian F, Danchin E, et al. (2004) High similarity between flanking regions of different microsatellites detected within each of two species of Lepidoptera: Parnassius apollo and Euphydryas aurinia. Molecular Ecology, 13, 1693-1700. (Pubitemid 38688918)
63. Meier PT, (2007) Fine spatial scale phenotypic divergence in wood frogs (Lithobates sylvaticus). Canadian Journal of Zoology, 85, 873-882. (Pubitemid 350145250)
64. Méndez M, Rosenbaum HC, Subramaniam A, Yackulic C, Bordino P, (2010) Isolation by environmental distance in mobile marine species: molecular ecology of franciscana dolphins at their southern range. Molecular Ecology, 19, 2212-2228.
65. Minor ES, Urban DL, (2007) Graph theory as a proxy for spatially explicit population models in conservation planning. Ecological Applications, 17, 1771-1782. (Pubitemid 351323495)
66. Nosil P, Egan SP, Funk DJ, Hoekstra H, (2009) Heterogeneous genomic differentation between walking-stick ecotypes: "isolation by adaptation" and multiple roles for divergent selection. Evolution, 62, 316-336. (Pubitemid 351294562)
67. Novembre J, Di Rienzo A, (2009) Spatial patterns of variation due to natural selection in humans. Nature Reviews Genetics, 10, 745-755.
68. Oksanen J, Kindt R, Legendre P, et al. (2009) Community Ecology Package, version 1.15-3.
69. Orizaola G, Laurila A, (2009) Microgeographic variation in temperature-induced plasticity in an isolated amphibian metapopulation. Evolutionary Ecology, 23, 979-991.
70. Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma R, Hedrick PW, (2010) Conservation genetics in transition to conservation genomics. Trends in Genetics, 26, 177-187.
71. Palsbøll PJ, Bérubé M, Allendorf FW, (2007) Identification of management units using population genetic data. Trends in Ecology & Evolution, 22, 11-16. (Pubitemid 44959169)
72. Paris M, Boyer S, Bonin A, et al. (2010) Genome scan in the mosquito Aedes rusticus: population structure and detection of positive selection after insecticide treatment. Molecular Ecology, 19, 325-337.
73. Peakall R, Smouse PE, (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288-295. (Pubitemid 43373825)
74. Pérez-Figueroa A, García-Pereira MJ, Saura M, Rolán-Úlvarez E, Caballero A, (2010) Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology, 23, 2267-2276.
75. Petranka JW, Holbrook CT, (2006) Wetland restoration for amphibians: should local sites be designed to support metapopulations or patchy populations? Restoration Ecology, 14, 404-411.
76. Petranka JW, Smith CK, Floyd Scott A, (2004) Identifying the minimal demographic unit for monitoring pond-breeding amphibians. Ecological Applications, 14, 1065-1078. (Pubitemid 39188057)
77. Piry S, Luikart G, Cornuet J-M, (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. The Journal of Heredity, 90, 502-503. (Pubitemid 29416458)
78. Raymond M, Rousset F, (1995) GENEPOP Version 1.2: population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
79. Rice KJ, Emery NC, (2003) Managing microevolution: restoration in the face of global change. Frontiers in Ecology and the Environment, 1, 469-478.
80. Richter-Boix A, Teplitsky C, Rogell B, Laurila A, (2010) Local selection modifies phenotypic divergence among Rana temporaria populations in the presence of gene flow. Molecular Ecology, 19, 716-731.
81. Riebler A, Held L, Stephan W, (2008) Bayesian variable selection for detecting adaptive genomic differences among populations. Genetics, 178, 1817-1829.
82. Rolshausen G, Segelbacher G, Hobson KA, Schaefer HM, (2009) Contemporary evolution of reproductive isolation and phenotypic divergence in sympatry along a migratory divide. Current Biology, 19, 2097-2101.
83. Rousset F, (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219-1228. (Pubitemid 27149123)
84. Rowe G, Beebee TJC, (2001) Polymerase chain reaction primers for microsatellite loci in the common frog Rana temporaria. Molecular Ecology Notes, 1, 6-7. (Pubitemid 33691829)
85. ST is still a useful measure of genetic differentiation-a comment on Jost's D. Molecular Ecology, 18, 2084-2087.
86. Schwartz MK, Luikart G, McKelvey KS, Cushman SA, (2010) Landscape genomics: a brief perspective. In: Spatial Complexity, Informatics, and Wildlife Conservation (eds, Cushman SA, Huettmann F,), pp. 165-174. Springer, New York.
87. Selkoe KA, Toonen RJ, (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecology Letters, 9, 615-629.
88. Semlitsch RD, (2002) Critical elements for biologically based recovery plans of aquatic-breeding amphibians. Conservation Biology, 16, 619-629. (Pubitemid 34592916)
89. Semlitsch RD, (2008) Differentiating migration and dispersal processes for pond-breeding amphibians. Journal of Wildlife Management, 72, 260-267. (Pubitemid 351171972)
90. Shi YB, Su Y, Li Q, Damjanovski S, (1998) Auto-regulation of thyroid hormone receptor genes during metamorphosis: roles in apoptosis and cell proliferation. International Journal of Developmental Biology, 42, 107-116. (Pubitemid 28109372)
91. Skelly DK, (2004) Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution, 58, 160-165. (Pubitemid 38355646)
92. Smith CT, Elfstrom CM, Seeb LW, Seeb JE, (2005) Use of sequence data from rainbow trout and Atlantic salmon for SNP detection in Pacific salmon. Molecular Ecology, 14, 4193-4203. (Pubitemid 44943748)
93. Spielman D, Brook BW, Frankham R, (2004) Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences USA, 101, 15261-15264. (Pubitemid 39391752)
94. Steiner CC, Weber JN, Hoekstra HE, (2007) Adaptive variation in beach mice produced by two interacting pigmentation genes. PLoS Biology, 5, e219.
95. Stockwell CA, Hendry AP, Kinnison MT, (2003) Contemporary evolution meets conservation biology. Trends in Ecology & Evolution, 18, 94-101. (Pubitemid 36072684)
96. Storz JF, Kelly JK, (2008) Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: insights from the deer mouse globin genes. Genetics, 180, 367-379.
97. Stuart SN, Chanson JS, Cox NA, et al. (2004) Status and trends of amphibian declines and extinctions worldwide. Science, 306, 1783-1786. (Pubitemid 39601397)
98. Valdés AM, Slatkin M, Freimer NB, (1993) Allele frequencies at microsatellite loci: the Stepwise Mutation model revisited. Genetics, 133, 737-749. (Pubitemid 23066575)
99. Väli Ü, Einarsson A, Waits L, Ellegren H, (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Molecular Ecology, 17, 3808-3817.
100. Van Buskirk J, Arioli M, (2005) Habitat specialization and adaptive phenotypic divergence of anuran populations. Journal of Evolutionary Biology, 18, 596-608. (Pubitemid 40654082)
101. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538. (Pubitemid 39147523)
102. Via S, (2009) Natural selection in action during speciation. Proceedings of the National Academy of Sciences USA, 106, 9939-9946.
103. Via S, West J, (2008) The genetic mosaic suggests a new role for hitchhiking in ecological speciation. Molecular Ecology, 17, 4334-4345.
104. 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 (Rana arvalis). Heredity, 86, 598-608. (Pubitemid 32818188)
105. Wang IJ, (2009) Fine-scale population structure in a desert amphibian: landscape genetics of the black toad (Bufo exsul). Molecular Ecology, 18, 3847-3856.
106. Warkman AS, Chen Y, (1998) Thyroid hormone induces a reprogramming of gene expression in the liver of premetamorphic Rana catesbeiana tadpoles. Wound Repair and Regeneration, 6, S-323-S-336.
107. Weir BS, Cockerham CC, (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358-1370. (Pubitemid 16277759)
108. Wellborn GA, Skelly DK, Werner EE, (1996) Mechanisms creating community structure across a freshwater habitat gradient. Annual Review of Ecology and Systematics, 27, 337-363.
109. Werner EE, Glennemeier KS, (1999) Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia, 1999, 1-12. (Pubitemid 129761318)
110. Wong J, Shi Y-B, (1995) Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. Journal of Biological Chemistry, 270, 18479-18483.
111. Yeaman S, Jarvis A, (2006) Regional heterogeneity and gene flow maintain variance in a quantitative trait within populations of lodgepole pine. Proceedings of the Royal Society B: Biological Sciences, 273, 1587-1593. (Pubitemid 46931043)
112. Zamudio KR, Wieczorek AM, (2007) Fine-scale spatial genetic structure and dispersal among spotted salamander (Ambystoma maculatum) breeding populations. Molecular Ecology, 16, 257-274. (Pubitemid 46058963)