Local adaptation with high gene flow: Temperature parameters drive adaptation to altitude in the common frog (Rana temporaria)

Molecular Ecology

Volumn 23, Issue 3, 2014, Pages 561-574

  Muir, A P ^a,c   Biek, R ^a   Thomas, R ^b   Mable, B K ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b ROYAL ZOOLOGICAL SOCIETY OF SCOTLAND   (United Kingdom)

^c INSTITUT UNIVERSITAIRE EUROPÉEN DE LA MER   (France)

Author keywords

climate; divergent selection; FST QST; phenotypic plasticity

Indexed keywords

RANA TEMPORARIA;

ADAPTATION; ALTITUDE; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CLIMATE; DIVERGENT SELECTION; FST-QST; GENE FLOW; GENETIC SELECTION; GENETICS; PHENOTYPE; PHENOTYPIC PLASTICITY; POPULATION GENETICS; QUANTITATIVE TRAIT; RANA TEMPORARIA; TEMPERATURE; UNITED KINGDOM;

CLIMATE; DIVERGENT SELECTION; FST-QST; PHENOTYPIC PLASTICITY;

ADAPTATION, PHYSIOLOGICAL; ALTITUDE; ANIMALS; GENE FLOW; GENETICS, POPULATION; MODELS, GENETIC; PHENOTYPE; QUANTITATIVE TRAIT, HERITABLE; RANA TEMPORARIA; SCOTLAND; SELECTION, GENETIC; TEMPERATURE;

EID: 84893016158     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12624     Document Type: Article

References (74)

1. Alho JS, Herczeg G, Laugen AT, et al,. (2010) Allen's rule revisited: quantitative genetics of extremity length in the common frog along a latitudinal gradient. Journal of Evolutionary Biology, 24, 59-70.
2. Allendorf FW, Luikart G, (2007) Conservation and the Genetics of Populations. Blackwell Publishing, Malden, Massachusetts, Oxford and Carlton, Victoria.
3. Altwegg R, Reyer H-U, (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872-882.
4. Barker JSF, Frydenberg J, Sarup P, Loeschcke V, (2011) Altitudinal and seasonal variation in microsatellite allele frequencies of Drosophila buzzatii. Journal of Evolutionary Biology, 24, 430-439.
5. Bates D, Maechler M, Bolker B, (2011) lme4: Linear Mixed-Effects Models Using S4 Classes, R package version 0.999375-42. http://cran.r-project.org/web/ packages/lme4/index.html.
6. Becker U, Colling G, Dostal P, Jakobsson A, Matthies D, (2006) Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia, 150, 506-518.
7. Berven KA, (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution, 52, 360-369.
8. 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.
9. Bridle JR, Vines TH, (2007) Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology & Evolution, 22, 140-147.
10. Briggs D, Smithson P, Addison K, Atkinson K, (1997) Fundamentals of the Physical Environment. Routledge, London and New York, New York.
11. Carey C, Alexander MA, (2003) Climate change and amphibian declines: is there a link? Diversity and Distributions, 9, 111-121.
12. Conover DO, Schultz ET, (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology and Evolution, 10, 248-252.
13. Cristescu ME, Constantin A, Bock DG, Caceres CE, Crease TJ, (2012) Speciation with gene flow and the genetics of habitat transitions. Molecular Ecology, 21, 1411-1422.
14. ST is misleading. Or is it? Molecular Ecology, 20, 1805-1812.
15. Edelaar P, Burraco P, Gomez-Mestre I, (2011) Comparisons between Q(ST) and F(ST) -how wrong have we been? Molecular Ecology, 20, 4830-4839.
16. Endler JA, (1977) Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, New Jersey.
17. Excoffier L, Lischer HEL, (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
18. Fukami T, Wardle DA, (2005) Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proceedings. Biological sciences / The Royal Society, 272, 2105-2115.
19. Galloway LF, Fenster CB, (2000) Population differentiation in an annual legume: local adaptation. Evolution, 54, 1173-1181.
20. Gomez-Mestre I, Tejedo M, (2004) Contrasting patterns of quantitative and neutral genetic variation in locally adapted populations of the natterjack toad, Bufo calamita. Evolution, 58, 2343-2352.
21. Gosner KL, (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16, 183-190.
22. Griffiths RA, Raper SJ, (1994) How many clumps are there in a mass of frog spawn? British Herpetological Bulletin, 50, 14-17.
23. Håkansson P, Loman J, (2004) Communal spawning in the common frog Rana temporaria-egg temperature and predation consequences. Ethology, 110, 665-680.
24. ST correlations. Evolution, 66, 867-881.
25. Hansen MM, Olivieri I, Waller DM, Nielsen EE, (2012) Monitoring adaptive genetic responses to environmental change. Molecular Ecology, 21, 1311-1329.
26. Inns H, (2009) Britain's Reptiles and Amphibians. WildGuides, Old Basing, UK.
27. Jost L, (2008) GST and its relatives do not measure differentiation. Molecular Ecology, 17, 4015-4026.
28. Kundzewicz ZW, Mata LJ, Arnell NW, et al,. (2007) Freshwater resources and their management. In: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (eds, Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, &, Hanson CE,), pp. 173-210. Cambridge University Press, Cambridge.
29. Lande R, (1976) The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genetical Research, 26, 221-235.
30. Laugen AT, Laurila A, Merilä J, (2002) Maternal and genetic contributions to geographical variation in Rana temporaria larval life-history traits. Biological Journal of the Linnean Society, 76, 61-70.
31. Laugen AT, Laurila A, Räsänen K, Merilä J, (2003) Latitudinal countergradient variation in the common frog (Rana temporaria) development rates-evidence for local adaptation. Journal of Evolutionary Biology, 16, 996-1005.
32. Laugen AT, Kruuk LEB, Laurila A, et al,. (2005) Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions. Genetical Research, 86, 161-170.
33. Laurila A, Seppa P, (1998) Multiple paternity in the common frog (Rana temporaria): genetic evidence from tadpole kin groups. Biological Journal of the Linnean Society, 63, 221-232.
34. Leinonen T, O'Hara RB, Cano JM, Merilä J, (2008) Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. Journal of Evolutionary Biology, 21, 1-17.
35. Lekberg Y, Roskilly B, Hendrick MF, et al,. (2012) Phenotypic and genetic differentiation among yellow monkeyflower populations from thermal and non-thermal soils in Yellowstone National Park. Oecologia, 170, 111-122.
36. Lind MI, Johansson F, (2007) The degree of adaptive phenotypic plasticity is correlated with the spatial environmental heterogeneity experienced by island populations of Rana temporaria. Journal of Evolutionary Biology, 20, 1288-1297.
37. Lind MI, Johansson F, (2011) Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained Rana temporaria populations. Journal of Evolutionary Biology, 24, 2696-2704.
38. Lind MI, Ingvarsson PK, Johansson H, Hall D, Johansson F, (2011) Gene flow and selection on phenotypic plasticity in an island system of Rana temporaria. Evolution, 65, 684-697.
39. Lindgren B, Laurila A, (2009a) Physiological variation along a geographical gradient: is growth rate correlated with routine metabolic rate in Rana temporaria tadpoles? Biological Journal of the Linnean Society, 98, 217-224.
40. Lindgren B, Laurila A, (2009b) Are high-latitude individuals superior competitors? A test with Rana temporaria tadpoles. Evolutionary Ecology, 24, 115-131.
41. Mantel N, Valand RS, (1970) A technique of nonparametric multivariate analysis. Biometrics, 26, 547-558.
42. McKay JK, Latta RG, (2002) Adaptive population divergence: markers, QTL and traits. Trends in Ecology & Evolution, 17, 285-291.
43. Meirmans PG, Hedrick PW, (2011) Assessing population structure: F(ST) and related measures. Molecular Ecology Resources, 11, 5-18.
44. Merilä J, Laurila A, Laugen AT, Rasanen K, Pahkala M, (2000a) Plasticity in age and size at metamorphosis in Rana temporaria-comparison of high and low latitude populations. Ecography, 23, 457-465.
45. Merilä J, Laurila A, Pahkala M, Räsänen K, Laugen AT, (2000b) Adaptive phenotypic plasticity in timing of metamorphosis in the common frog Rana temporaria. Ecoscience, 7, 18-24.
46. Miaud C, Merilä J, (2001) Local adaptation or environmental induction? Causes of population differentiation in alpine amphibians. Biota, 2, 31-50.
47. Miller MR, Brunelli JP, Wheeler PA, et al,. (2011) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Molecular Ecology, 21, 237-249.
48. Muir AP, Thomas R, Biek R, Mable BK, (2013) Using genetic variation to infer associations with climate in the common frog, Rana temporaria. Molecular Ecology, 22, 3737-3751.
49. Narum SR, Campbell NR, Meyer KA, Miller MR, Hardy RW, (2013) Thermal adaptation and acclimation of ectotherms from differing aquatic climates. Molecular Ecology, 22, 3090-3097.
50. North A, Pennanen J, Ovaskainen O, Laine A-L, (2010) Local adaptation in a changing world: the roles of gene-flow, mutation, and sexual reproduction. Evolution, 66, 79-89.
51. O'Hara RB, Merilä J, (2005) Bias and precision in QST estimates: problems and some solutions. Genetics, 171, 1331-1339.
52. Orizaola G, Quintela M, Laurila A, (2010) Climatic adaptation in an isolated and genetically impoverished amphibian population. Ecography, 33, 730-737.
53. Orizaola G, Dahl E, Nicieza AG, Laurila A, (2013) Larval life history and anti-predator strategies are affected by breeding phenology in an amphibian. Oecologia, 171, 873-881.
54. Ovaskainen O, Karhunen M, Zheng C, Arias JMC, Merilä J, (2011) A new method to uncover signatures of divergent and stabilizing selection in quantitative traits. Genetics, 189, 621-632.
55. Palo JU, O'Hara RB, Laugen AT, Laurila A, Primmer CR, (2003) Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Molecular Ecology, 12, 1963-1978.
56. R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
57. Raffel TR, Rohr JR, Kiesecker JM, Hudson PJ, (2006) Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology, 20, 819-828.
58. 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.
59. Richter-Boix A, Quintela M, Segelbacher G, Laurila A, (2011) Genetic analysis of differentiation among breeding ponds reveals a candidate gene for local adaptation in Rana arvalis. Molecular Ecology, 20, 1582-1600.
60. Richter-Boix A, Quintela M, Kierczak M, Franch M, Laurila A, (2013) Fine-grained adaptive divergence in an amphibian: genetic basis of phenotypic divergence and the role of nonrandom gene flow in restricting effective migration among wetlands. Molecular Ecology, 22, 1322-1340.
61. Savolainen O, Pyhäjärvi T, Knürr T, (2007) Gene flow and local adaptation in trees. Annual Review of Ecology Evolution and Systematics, 38, 595-619.
62. Sears MW, (2005) Resting metabolic expenditure as a potential source of variation in growth rates of the sagebrush lizard. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 140, 171-177.
63. Skelly DK, (2004) Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution, 58, 160-165.
64. Thompson DBA, Brown A, (1992) Biodiversity in montane Britain: habitat variation, vegetation diversity and some objectives for conservation. Biodiversity and Conservation, 1, 179-208.
65. Torres-Dowdall J, Handelsman CA, Reznick DN, Ghalambor CK, (2012) Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata). Evolution, 66, 3432-3443.
66. Trivedi MR, Morecroft MD, Berry PM, Dawson TP, (2008) Potential effects of climate change on plant communities in three montane nature reserves in Scotland, UK. Biological Conservation, 141, 1665-1675.
67. Tukey JW, (1953) Some selected quick and easy methods of statistical analysis. Transactions of the New York Academy of Sciences, 16, 88-97.
68. Urban MC, (2010) Microgeographic adaptations of spotted salamander morphological defenses in response to a predaceous salamander and beetle. Oikos, 119, 646-658.
69. Van Buskirk J, Steiner UK, (2009) The fitness costs of developmental canalization and plasticity. Journal of Evolutionary Biology, 22, 852-860.
70. Via S, (1993) Adaptive phenotypic plasticity: target or by-product of selection in a variable environment? The American Naturalist, 142, 352-365.
71. Via S, Lande R, (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 505-522.
72. Vieites DR, Nieto-roma S, Barluenga M, et al,. (2004) Post-mating clutch piracy in an amphibian. Nature, 431, 305-308.
73. Whitlock MC, (2008) Evolutionary inference from QST. Molecular Ecology, 17, 1885-1896.
74. ST. Genetics, 183, 1055-1063.