Abstract
Studies of genetic correlations between traits that ostensibly channel the path of evolution away from the direction of natural selection require information on key aspects such as ancestral phenotypes, the duration of adaptive evolution, the direction of natural selection, and genetic covariances. In this study we provide such information in a frog population system. We studied adaptation in life history traits to pool drying in frog populations on islands of known age, which have been colonized from a mainland population. The island populations show strong local adaptation in development time and size. We found that the first eigenvector of the variance–covariance matrix (g max) had changed between ancestral mainland populations and newly established island populations. Interestingly, there was no divergence in g max among island populations that differed in their local adaptation in development time and size. Thus, a major change in the genetic covariance of life-history traits occurred in the colonization of the island system, but subsequent local adaptation in development time took place despite the constraints imposed by the genetic covariance structure.
Similar content being viewed by others
References
Altwegg R, Reyer HU (2003) Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57:872–882
Arnold SJ, Phillips PC (1999) Hierarchical comparison of genetic variance-covariance matrices. II. Coastal-inland divergence in the garter snake, Thamnophis elegans. Evolution 53:1516–1527
Arnold SJ, Burger R, Holenhole PA, Beverley CA, Jones AG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62:2451–2461
Ball SL, Baker RL (1996) Predator-induced life history changes: antipredatore behavior costs or facultative life history shifts? Ecology 77:1116–1124
Bégin M, Roff DA (2003) The constancy of the G matrix through species divergence and the effects of quantitative genetic constraints on phenotypic evolution: a case study in crickets. Evolution 57:1107–1120
Berner D, Adams DC, Grandchamp A-C, Hendry AP (2008) Natural selection drives patterns of lake –stream divergence in stickleback foraging morphology. J Evol Biol 21:1653–1665
Berner D, Stutz WE, Bolnick DI (2010) Foarging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution 64:2265–2277
Berven KA (1990) Factors affecting population fluctuations in larval and adult stages of the wood frog (R. sylvatica). Ecology 71:1599–1608
Blows MW, Higgie M (2003) Genetic constraints on the evolution of mate recognition under Natural Selection. Am Nat 161:240–253
Blows MW, Hoffmann AA (2005) A reassessment of genetic limits to evolutionary change. Ecology 86:1371–1384
Cano JM, Laurila A, Palo J, Merilä J (2004) Population differentiation in G matrix structure due to natural selection in R. temporaria. Evolution 58:2013–2020
Chenoweth SF, Rundle HD, Blows MW (2010) The contribution of selection and genetic constraints to phenotypic divergence. Am Nat 175:186–196
Doroszuk A, Wojewodzic MW, Gort G, Kammenga JE (2008) Rapid divergence of genetic variance-covariance matrix within a natural population. Am Nat 171:291–304
Elmberg J (1991a) Factors affecting male yearly mating success in the common frog, R. temporaria. Beh Ecol Sociobiol 28:125–131
Elmberg J (1991b) Ovarian cyclicity and fecundity in boreal common frogs R. temporaria L. along a climatic gradient. Funct Ecol 5:340–350
Eroukhmanoff F (2009) Just how much is the G-matrix actually constraining adaptation? Evol Biol 36:323–326
Eroukhmanoff F, Svensson EI (2008) Phenotypic integration and conserved covariance structure in calopterygid damselflies. J Evol Biol 21:514–526
Eroukhmanoff F, Svensson EI (2011) Evolution and stability of the G-matrix during colonization of a novel envirnonment. J Evol Biol 24:1363–1373
Eroukhmanoff F, Outomuro D, Ochoran FJ, Svensson EI (2009) Patterns of phenotypic divergence in wing covariance structure of calopterygid damselflies. Evol Biol 36:214–224
Gasc J et al (1997) Atlas of amphibians and reptiles in Europe, Societas Europea Herpetologica & Museum National d’Histoire Naturelle, Paris
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Heredity 86:485–486
Hadfield JD (2010) MCMC Methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22
Hansen TF, Houle D (2008) Measuring and comparing evolvability and constraints in multivariate characters. J Evol Biol 21:1201–1219
Hine E, Chenoweth S, Rundle HD, Blows MW (2009) Characterizing the evolution of genetic covariance tensors. Phil Trans R Soc B 364:1567–1578
Johansson F, Hjelm J, Giles BE (2005) Life history and morphology of R. temporaria in response to pool permanence. Evol Ecol Res 7:1025–1038
Jones AG, Arnold SJ, Burger R (2003) Stability of the G-matrix in a population experiencing pleitropic mutation, stabilizing selection and genetic drift. Evolution 57:1747–1760
Lande R (1979) Quantitative genetic analysis of multivariate evolution, applied to brain-body size allometry. Evolution 33:402–416
Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226
Laurila A, Kujasalo J (1999) Habitat duration, predation risk and phenotypic plasticity in common frog (R. temporaria) tadpoles. J Anim Ecol 68:1123–1132
Laurila A, Seppä P (1998) Multiple paternity in the common frog (R. temporaria): genetic evidence from tadpole kin groups. Biol J Linn Soc 63:221–232
Lind MI (2009) Phenotypic plasticity and local adaptation in island populations of R. temporaria. PhD Thesis, Umeå University
Lind MI, Johansson F (2007) The degree of adaptive phenotypic plasticity is correlated with the spatial environmental heterogeneity experienced by island populations of R. temporaria. J Evol Biol 20:1288–1297
Lind MI, Johansson F (2011) Testing the role of phenotypic plasticity for local adaptation: growth and development in time-constrained R. temporaria populations. J Evol Biol Online Early. doi: 10.1111/j.1420-9101.2011.02393.x
Lind MI, Persbo F, Johansson F (2008) Pool desiccation and developmental thresholds in the common frog, R. temporaria. Proc R Soc B 275:1071–1080
Lind MI, Ingvarsson PK, Johansson H, Hall D, Johansson F (2011) Gene flow and selection on phenotypic plasticity in an island system. Evolution 65:684–697
Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates Inc, Sunderland
Marroig G, Cheverud JM (2005) Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in new world monkeys. Evolution 59:1128–1142
McGuigan K (2006) Studying evolution using multivariate quantitative genetics. Mol Ecol 15:883–896
McGuigan K, Chenoweth SF, Blows MW (2005) Phenotypic divergence along lines of genetic variance. Am Nat 165:32–43
Merilä J, Björklund M (1999) Population divergence and morphometric integration in the greenfinch (Carduelis chloris)—evolution against the lines of least resistance. J Evol Biol 12:103–112
Merilä J, Sheldon BC (1999) Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109
Phillips PC, Arnold SJ (1999) Hierarchical comparison of genetic variance–covariance matrices. I. Using the Flury hierarchy. Evolution 53:1506–1515
Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecol Lett 6:265–272
Plummer M, Best N, Cowles K, Vines K (2006) CODA: convergence diagnosis and output analysis for MCMC. R News 6:7–11
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, New York
Roff D (2002) Comparing G matrices: a MANOVA approach. Evolution 56:1286–1291
Roff DA, Mousseau T, Møller AP, deLope F, Saino N (2004) Geographic variation in the G matrices of wild populations of the barn swallow. Heredity 93:8–14
Rowe L, Ludwig D (1991) Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72:413–427
Schluter D (1996) Adaptive radiation along genetic lines of least resistance. Evolution 50:1766–1774
Sgro CM, Blows MW (2004) The genetic covariance among clinal environments after adaptation to an environmental gradient in Drosophila serrate. Genetics 167:1281–1291
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Steppan SJ, Phillips PC, Houle D (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol 17:320–327
Wilson AJ et al (2009) An ecologist guide to the animal model. J Anim Ecol 79:13–26
Acknowledgments
We thank J. Almfelt for help with egg collection and laboratory experiments, and two anonymous reviewers for very constructive comments that improved this article. The Swedish Research Council and the Swedish Research Council FORMAS funded the research.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
See Table 3.
Rights and permissions
About this article
Cite this article
Johansson, F., Lind, M.I., Ingvarsson, P.K. et al. Evolution of the G-matrix in life history traits in the common frog during a recent colonisation of an island system. Evol Ecol 26, 863–878 (2012). https://doi.org/10.1007/s10682-011-9542-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-011-9542-2