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Ecological adaptation drives wood frog population divergence in life history traits

  • Adams DC, Church JO (2008) Amphibians do not follow Bergmann’s rule. Evol: Int J Org Evol 62(2):413–420

    Article  Google Scholar 

  • Alho J, Herczeg G, Laugen A, Räsänen K, Laurila A, Merilä J (2011) Allen’s rule revisited: quantitative genetics of extremity length in the common frog along a latitudinal gradient. J Evol Biol 24(1):59–70

    CAS  PubMed  Article  Google Scholar 

  • Allen JA (1877) The influence of physical conditions in the genesis of species. Radic Rev 1:108–140

    Google Scholar 

  • Amado TF, Bidau CJ, Olalla-Tárraga MÁ (2019) Geographic variation of body size in New World anurans: energy and water in a balance. Ecography 42(3):456–466

    Article  Google Scholar 

  • Ashton KG (2002) Do amphibians follow Bergmann’s rule? Can J Zool 80(4):708–716

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Belden LK, Rubbo MJ, Wingfield JC, Kiesecker JM (2007) Searching for the physiological mechanism of density dependence: does corticosterone regulate tadpole responses to density? Physiol Biochem Zool 80(4):444–451

    CAS  PubMed  Article  Google Scholar 

  • Berven KA (1982a) The genetic basis of altitudinal variation in the wood frog Rana sylvatica II. An experimental analysis of larval development. Oecologia 52(3):360–369

    PubMed  Article  Google Scholar 

  • Berven KA (1982b) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution 36(5):962–983

    PubMed  Google Scholar 

  • Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71(4):1599–1608

    Article  Google Scholar 

  • Berven KA (2009) Density dependence in the terrestrial stage of wood frogs: evidence from a 21-year population study. Copeia 2009(2):328–338

    Article  Google Scholar 

  • Berven KA, Gill DE (1983) Interpreting geographic-variation in life-history traits. Am Zool 23(1):85–97

    Article  Google Scholar 

  • Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5(2):117–129

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Bjornstad ON (2020) ncf: spatial covariance functions. R package version 1.2-9. https://cran.r-project.org/package=ncf

  • Castellano S, Balletto E (2002) Is the partial Mantel test inadequate? Evolution 56(9):1871–1873

    PubMed  Article  PubMed Central  Google Scholar 

  • Chaparro-Pedraza PC, de Roos AM (2020) Density-dependent effects of mortality on the optimal body size to shift habitat: Why smaller is better despite increased mortality risk. Evolution 74(5):831–841

    PubMed  PubMed Central  Article  Google Scholar 

  • Conover DO, Schultz ET (1995) Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol Evol 10(6):248–252

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Cordero GA, Epps CW (2012) From desert to rainforest: phenotypic variation in functionally important traits of bushy-tailed woodrats (Neotoma cinerea) across two climatic extremes. J Mamm Evol 19(2):135–153

    Article  Google Scholar 

  • Costanzo JP, do Amaral MCF, Rosendale AJ, Lee RE (2013) Hibernation physiology, freezing adaptation and extreme freeze tolerance in a northern population of the wood frog. J Exp Biol 216(18):3461–3473

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Crespi EJ, Warne RW (2013) Environmental conditions experienced during the tadpole stage alter post-metamorphic glucocorticoid response to stress in an amphibian. Integr Comp Biol 53(6):989–1001

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Dahl E, Orizaola G, Nicieza AG, Laurila A (2012) Time constraints and flexibility of growth strategies: geographic variation in catch‐up growth responses in amphibian larvae. J Anim Ecol 81(6):1233–1243

    PubMed  Article  PubMed Central  Google Scholar 

  • Davenport JM, Hossack BR (2016) Reevaluating geographic variation in life‐history traits of a widespread Nearctic amphibian. J Zool 299(4):304–310

    Article  Google Scholar 

  • Denver RJ (1997) Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31(2):169–179

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • DeWitt TJ, Scheiner SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, New York, NY USA

  • Dorcas ME, Gibbons JW (2008) Frogs and Toads of the Southeast. University of Georgia Press, Athens, GA, USA

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G et al. (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36(1):27–46

    Article  Google Scholar 

  • Duncan SI, Crespi EJ, Mattheus NM, Rissler LJ (2015) History matters more when explaining genetic diversity within the context of the core–periphery hypothesis. Mol Ecol 24(16):4323–4336

    PubMed  Article  PubMed Central  Google Scholar 

  • Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Diversity Distrib 17(1):43–57

    Article  Google Scholar 

  • Fitzpatrick MJ, Zuckerberg B, Pauli JN, Kearney MR, Thompson KL, Werner LC et al. (2019) Modeling the distribution of niche space and risk for a freeze‐tolerant ectotherm, Lithobates sylvaticus. Ecosphere 10(7):e02788

    Article  Google Scholar 

  • Fox J, Weisberg S (2019) An R Companion to Applied Regression, 3rd Edition. Sage, Thousand Oaks, CA

  • GBIF.org (2014) GBIF Occurrence Download. https://doi.org/10.15468/dl.e3k4ag

  • Gouveia SF, Correia I (2016) Geographical clines of body size in terrestrial amphibians: water conservation hypothesis revisited. J Biogeogr 43(10):2075–2084

    Article  Google Scholar 

  • Hahn DA, Martin AR, Porter SD (2008) Body size, but not cooling rate, affects supercooling points in the red imported fire ant, Solenopsis invicta. Environ Entomol 37(5):1074–1080

    PubMed  Article  Google Scholar 

  • Hangartner S, Laurila A, Rasanen K (2012) Adaptive divergence in moor frog (Rana arvalis) populations along an acidification gradient: inferences from Q(st) -F(st) correlations. Evolution 66(3):867–881

    PubMed  PubMed Central  Article  Google Scholar 

  • Hijmans R, Cameron S, Parra J, Jones P, Jarvis A, Richardson K (2005) WorldClim version 1.3. University of California, Berkeley

    Google Scholar 

  • Holderegger R, Kamm U, Gugerli F (2006) Adaptive vs. neutral genetic diversity: implications for landscape genetics. Landsc Ecol 21(6):797–807

    Article  Google Scholar 

  • Kawakami T, Morgan TJ, Nippert JB, Ocheltree TW, Keith R, Dhakal P et al. (2011) Natural selection drives clinal life history patterns in the perennial sunflower species, Helianthus maximiliani. Mol Ecol 20(11):2318–2328

    PubMed  Article  Google Scholar 

  • Kierepka E, Latch E (2015) Performance of partial statistics in individual‐based landscape genetics. Mol Ecol Resour 15(3):512–525

    CAS  PubMed  Article  Google Scholar 

  • Kingsolver JG, Diamond SE (2011) Phenotypic selection in natural populations: what limits directional selection? Am Naturalist 177(3):346–357

    Article  Google Scholar 

  • Kingsolver JG, Pfennig DW (2004) Individual-level selection as a cause of cope’s rule of phyletic size increase. Evolution 58(7):1608–1612

    PubMed  Article  Google Scholar 

  • Laugen AT, Laurila A, Jönsson KI, Söderman F, Merilä J (2005) Do common frogs (Rana temporaria) follow Bergmann’s rule? Evol Ecol Res 7(5):717–731

    Google Scholar 

  • Laugen AT, Laurila A, Räsänen K, Merilä J (2003) Latitudinal countergradient variation in the common frog (Rana temporaria) development rates–evidence for local adaptation. J Evol Biol 16(5):996–1005

    CAS  PubMed  Article  Google Scholar 

  • Laurila A, Karttunen S, Merila J (2002) Adaptive phenotypic plasticity and genetics of larval life histories in two Rana temporaria populations. Evolution 56(3):617–627

    PubMed  Article  Google Scholar 

  • Lee-Yaw JA, Irwin JT, Green DM (2008) Postglacial range expansion from northern refugia by the wood frog, Rana sylvatica. Mol Ecol 17(3):867–884

    CAS  PubMed  Article  Google Scholar 

  • Leinonen T, Cano JM, Mäkinen H, Merilä J (2006) Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. J Evol Biol 19(6):1803–1812

    CAS  PubMed  Article  Google Scholar 

  • Leinonen T, McCairns RJ, O’Hara RB, Merila J (2013a) Q(ST)-F(ST) comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14(3):179–190

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Leinonen T, McCairns RS, O’hara RB, Merilä J (2013b) Q ST–F ST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14(3):179

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lenker MA, Savage AE, Becker CG, Rodriguez D, Zamudio KR (2014) Batrachochytrium dendrobatidis infection dynamics vary seasonally in upstate New York, USA. Dis Aquat Organ 111(1):51–60

    PubMed  Article  Google Scholar 

  • Lind M, Johansson F (2011) Testing the role of phenotypic plasticity for local adaptation: growth and development in time‐constrained Rana temporaria populations. J Evol Biol 24(12):2696–2704

    CAS  PubMed  Article  Google Scholar 

  • 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(3):684–697

    PubMed  Article  Google Scholar 

  • Lindgren B, Laurila A (2009) Physiological variation along a geographical gradient: is growth rate correlated with routine metabolic rate in Rana temporaria tadpoles? Biol J Linn Soc 98(1):217–224

    Article  Google Scholar 

  • Lomolino MV, Heaney LR (2004) Frontiers of biogeography: new directions in the geography of nature. Sinauer Associates, Sunderland, MA, USA

  • Manis ML, Claussen DL (1986) Environmental and genetic influences on the thermal physiology of Rana sylvatica. J Therm Biol 11(1):31–36

    Article  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27(2 Part 1):209–220

    CAS  Google Scholar 

  • Martof BS, Humphries RL (1959) Geographic variation in the wood frog Rana sylvatica. Am Midl Naturalist 61(2):350–389

    Article  Google Scholar 

  • Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14(6):892–903

    Article  Google Scholar 

  • Merilä J, Laurila A, Laugen AT, Räsänen K, Pahkala M (2000) Plasticity in age and size at metamorphosis in Rana temporaria‐comparison of high and low latitude populations. Ecography 23(4):457–465

    Article  Google Scholar 

  • Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8(11):845–856

    CAS  Article  Google Scholar 

  • Morrison C, Hero JM (2003) Geographic variation in life‐history characteristics of amphibians: a review. J Anim Ecol 72(2):270–279

    Article  Google Scholar 

  • Mueller LD (1997) Theoretical and empirical examination of density-dependent selection. Annu Rev Ecol Syst 28(1):269–288

    Article  Google Scholar 

  • Muir AP, Biek R, Thomas R, Mable BK (2014) Local adaptation with high gene flow: temperature parameters drive adaptation to altitude in the common frog (Rana temporaria). Mol Ecol 23(3):561–574

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Nosil P, Vines TH, Funk DJ (2005) Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59(4):705–719

    PubMed  PubMed Central  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara R et al. (2019) vegan: Community Ecology Package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan

  • Olalla-Tárraga MÁ, Rodríguez MÁ (2007) Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann’s rule, urodeles its converse. Glob Ecol Biogeogr 16(5):606–617

    Article  Google Scholar 

  • Orizaola G, Quintela M, Laurila A (2010) Climatic adaptation in an isolated and genetically impoverished amphibian population. Ecography 33(4):730–737

    Article  Google Scholar 

  • Padgham M, Sumner MD (2020) geodist: fast, dependency-free geodesic distance calculations. R package version 0.0.6. https://CRAN.R-project.org/package=geodist

  • Palo JU, O’Hara RB, Laugen AT, Laurila A, Primmer CR, Merila J (2003) Latitudinal divergence of common frog (Rana temporaria) life history traits by natural selection: evidence from a comparison of molecular and quantitative genetic data. Mol Ecol 12(7):1963–1978

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Peters RH, Peters RH (1986) The ecological implications of body size, vol 2. Cambridge University Press, New York, NY, USA

  • Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190(3-4):231–259

    Article  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore, MA, USA

  • Powell R, Conant R, Collins JT (2016) Peterson field guide to reptiles and amphibians of eastern and central North America. Houghton Mifflin Harcourt, New York, NY, USA

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. https://www.R-project.org/

  • Raufaste N, Rousset F (2001) Are partial Mantel tests adequate? Evolution 55(8):1703–1705

    CAS  PubMed  Article  Google Scholar 

  • Rice KC, Jung RE (2004) Water-quality and amphibian population data for Maryland, Washington, DC, and Virginia, 2001–2004. US Geological Survey

  • 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. Mol Ecol 22(5):1322–1340

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 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. Mol Ecol 19(4):716–731

    PubMed  Article  Google Scholar 

  • Richter‐Boix A, Katzenberger M, Duarte H, Quintela M, Tejedo M, Laurila A (2015) Local divergence of thermal reaction norms among amphibian populations is affected by pond temperature variation. Evolution 69(8):2210–2226

    PubMed  Article  Google Scholar 

  • Rissler LJ (2016) Union of phylogeography and landscape genetics. Proc Natl Acad Sci USA 113(29):8079–8086

    CAS  PubMed  Article  Google Scholar 

  • Roff D (1980) Optimizing development time in a seasonal environment: the ‘ups and downs’ of clinal variation. Oecologia 45(2):202–208

    PubMed  Article  Google Scholar 

  • Santos M, Borash DJ, Joshi A, Bounlutay N, Mueller LD (1997) Density‐dependent natural selection in Drosophila: evolution of growth rate and body size. Evolution 51(2):420–432

    PubMed  Google Scholar 

  • Schemske DW, Bierzychudek P (2007) Spatial differentiation for flower color in the desert annual Linanthus parryae: was Wright right? Evol: Int J Org Evol 61(11):2528–2543

    Article  Google Scholar 

  • Schueler FW (1975) Geographic variation in the size of Rana septentrionalis in Quebec, Ontario, and Manitoba. J Herpetol 9(2):177–185

    Article  Google Scholar 

  • Semlitsch RD, Scott DE, Pechmann JHK (1988) Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum. Ecology 69(1):184–192

    Article  Google Scholar 

  • Shafer AB, Wolf JB (2013) Widespread evidence for incipient ecological speciation: a meta‐analysis of isolation‐by‐ecology. Ecol Lett 16(7):940–950

    PubMed  PubMed Central  Article  Google Scholar 

  • Sheridan JA, Caruso NM, Apodaca JJ, Rissler LJ (2018) Shifts in frog size and phenology: testing predictions of climate change on a widespread anuran using data from prior to rapid climate warming. Ecol Evol 8(2):1316–1327

    PubMed  Article  PubMed Central  Google Scholar 

  • Smith-Gill SJ, Berven KA (1979) Predicting amphibian metamorphosis. Am Naturalist 113(4):563–585

    Article  Google Scholar 

  • Spitze K (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics 135(2):367–374

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Stevens CE, Paszkowski CA (2004) Using chorus-size ranks from call surveys to estimate reproductive activity of the wood frog (Rana sylvatica). J Herpetol 38(3):404–410

    Article  Google Scholar 

  • Therneau TM (2020) coxme: Mixed effects cox models. R package version 2.2-16. https://CRAN.R-project.org/package=coxme

  • Thomassen HA, Cheviron ZA, Freedman AH, Harrigan RJ, Wayne RK, Smith TB (2010) Spatial modelling and landscape‐level approaches for visualizing intra‐specific variation. Mol Ecol 19(17):3532–3548

    PubMed  Article  Google Scholar 

  • Van Buskirk J (2017) Spatially heterogeneous selection in nature favors phenotypic plasticity in anuran larvae. Evolution 71(6):1670–1685

    PubMed  Article  PubMed Central  Google Scholar 

  • Venables W, Ripley B (2002) Modern Applied Statistics with S. 4th Edition. Springer, New York, NY, USA

  • Wang IJ, Bradburd GS (2014) Isolation by environment. Mol Ecol 23(23):5649–5662

    Article  Google Scholar 

  • Wang IJ, Summers K (2010) Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison‐dart frog. Mol Ecol 19(3):447–458

    PubMed  Article  PubMed Central  Google Scholar 

  • Warne RW, Crespi EJ (2015) Larval growth rate and sex determine resource allocation and stress responsiveness across life stages in juvenile frogs. J Exp Zool A Ecol Genet Physiol 323(3):191–201

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Weber MM, Stevens RD, Diniz‐Filho JAF, Grelle CEV (2017) Is there a correlation between abundance and environmental suitability derived from ecological niche modelling? A meta‐analysis. Ecography 40(7):817–828

    Article  Google Scholar 

  • Weir L (2001) NAAMP unified protocol: call surveys. North American Amphibian Monitoring Program. Patuxtent Wildlife Research Center, Patuxtent, MA, USA

  • Whitlock MC (2008) Evolutionary inference from QST. Mol Ecol 17(8):1885–1896

    PubMed  Article  PubMed Central  Google Scholar 

  • Whitlock MC, Guillaume F (2009) Testing for spatially divergent selection: comparing QST to FST. Genetics 183(3):1055–1063

    PubMed  PubMed Central  Article  Google Scholar 

  • Whitlock MC, Phillips PC (2000) The exquisite corpse: a shifting view of the shifting balance. Trends Ecol Evol 15(9):347–348

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Wilbur HM (1976) Density‐dependent aspects of metamorphosis in Ambystoma and Rana sylvatica. Ecology 57(6):1289–1296

    Article  Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182(4119):1305–1314

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28(2):114

    CAS  PubMed  PubMed Central  Google Scholar 


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