Evolutionary Biology

, Volume 42, Issue 4, pp 473–482 | Cite as

Plastic Responses to Temperature Versus Local Adaptation at the Cold Extreme of the Climate Gradient

Research Article

Abstract

Climate is a strong selection agent at high elevations, but experimental examinations of how animals exclusive of highlands cope with its variation are scarce. We analysed temperature-induced variation of early ontogenetic traits in the alpine grasshopper Chorthippus cazurroi, and compared populations from the elevational extremes of the species distribution under laboratory conditions spanning natural temperature ranges. Neither elevation of origin, nor different growing temperatures, had a direct effect on nymph body size, but both factors contributed to size at hatching indirectly, via their effect on the duration of embryo development. Large emerging nymphs had a consistently greater survival, although small and fast-developing nymphs from highlands also performed well at low temperatures. Viability selection favoured fast-developing phenotypes in conditions in which plasticity delayed development, in a typical countergradient pattern. Growth in the successive stage did not compensate for slow development at hatching, thus responses at this early stage have potential long-lasting consequences. Although phenotypic selection during early development certifies the strength of selection imposed by cold temperatures in the laboratory, elevation clines of body size did not emerge in either nymphs or the wild parental generation. Differentiation in the wild may be levelled out by fecundity selection for large sizes, drift and gene flow resulting from the fragmentation and proximity of populations, or by micro-climatic differences that reduce the likelihood of directional selection. There is therefore potential for local adaptation to temperature, but a series of conditions typical of alpine environments and ectotherms may impair, confound or constrain full differentiation along the gradient.

Keywords

Alpine fauna Body size Countergradient selection Development Phenotypic selection Selection gradients 

Supplementary material

11692_2015_9341_MOESM1_ESM.doc (140 kb)
Supplementary material 1 (DOC 140 kb)

References

  1. Aarssen, L. W., & Clauss, M. J. (1992). Genotypic variation in fecundity allocation in Arabidopsis thaliana. Journal of Ecology, 80, 109–114.CrossRefGoogle Scholar
  2. Altwegg, R., & Reyer, H.-U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution, 57, 872–882.CrossRefPubMedGoogle Scholar
  3. Álvarez, D., Cano, J. M., & Nicieza, A. G. (2006). Microgeographic variation in metabolic rate and energy storage of brown trout: Countergradient selection or thermal sensitivity? Evolutionary Ecology, 20, 345–363.CrossRefGoogle Scholar
  4. Angilletta, M. J., Steury, T. D., & Sears, M. W. (2004). Temperature, growth rate, and body size in ectotherms: Fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44, 498–509.CrossRefPubMedGoogle Scholar
  5. Arendt, J. D. (1997). Adaptive intrinsic growth rates: An integration across taxa. The Quarterly Review of Biology, 72, 149–177.CrossRefGoogle Scholar
  6. Atkinson, D. (1995). Effects of temperature on the size of aquatic ectotherms: Exceptions to the general rule. Journal of Thermal Biology, 20, 61–74.CrossRefGoogle Scholar
  7. Barton, N. H. (1999). Clines in polygenic traits. Genetics Research, 74, 223–236.CrossRefGoogle Scholar
  8. Bennington, C. C., & Thayne, W. V. (1994). Use and misuse of mixed model analysis of variance in ecological studies. Ecology, 75, 717–722.CrossRefGoogle Scholar
  9. Benton, T. G., & Grant, A. (1999). Elasticity analysis as an important tool in evolutionary and population ecology. Trends in Ecology & Evolution, 14, 467–471.CrossRefGoogle Scholar
  10. Bernardo, J. (1993). Determinants of maturation in animals. Trends in Ecology & Evolution, 8, 166–173.CrossRefGoogle Scholar
  11. Berner, D., & Blanckenhorn, W. U. (2006). Grasshopper ontogeny in relation to time constraints: Adaptive divergence and stasis. Journal of Animal Ecology, 7, 130–139.CrossRefGoogle Scholar
  12. Berner, D., & Blanckenhorn, W. U. (2007). An ontogenetic perspective on the relationship between age and size at maturity. Functional Ecology, 21, 505–512.CrossRefGoogle Scholar
  13. Berner, D., Körner, C., & Blanckenhorn, W. U. (2004). Grasshopper populations across 2000 m of altitude: Is there life history adaptation? Ecography, 27, 733–740.CrossRefGoogle Scholar
  14. Berven, K. A., & Gill, D. E. (1983). Interpreting geographic variation in life-history traits. American Zoologist, 23, 85–97.CrossRefGoogle Scholar
  15. Byers, S. G., Papst, W., & Hoffmann, A. A. (2007). Local adaptation and cogradient selection in the alpine plant, Poa hiemata, along a narrow altitudinal gradient. Evolution, 61, 2925–2941.CrossRefGoogle Scholar
  16. Conover, D. O., Duffy, T. A., & Hice, L. A. (2009). The covariance between genetic and environmental influences across ecological gradients. Annals of the New York Academy of Sciences, 1168, 100–129.CrossRefPubMedGoogle Scholar
  17. Conover, D. O., & Heins, S. W. (1987). Adaptive variation in environmental and genetic sex determination in a fish. Nature, 326, 496–498.CrossRefPubMedGoogle Scholar
  18. Conover, D. O., & Schultz, E. T. (1995). Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution, 10, 248–252.CrossRefGoogle Scholar
  19. D’Amico, L. J., Davidovitz, G., & Nijhout, H. F. (2001). The developmental and physiological basis of body size evolution in an insect. Proceedings of the Royal Society B: Biological Sciences, 268, 1589–1593.PubMedCentralCrossRefPubMedGoogle Scholar
  20. DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13, 77–81.CrossRefGoogle Scholar
  21. Dingle, H., Mousseau, T. A., & Scott, S. M. (1990). Altitudinal variation in life cycle syndromes of California populations of the grasshopper, Melanoplus sanguinipes (F.). Oecologia, 84, 199–206.CrossRefGoogle Scholar
  22. Ghalambor, C. K., McKay, K. J., Carroll, S. P., & Reznick, D. N. (2007). Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology, 21, 394–407.CrossRefGoogle Scholar
  23. Hatle, J. D., Crowley, M. C., Andrews, A. L., & Juliano, S. A. (2002). Geographic variation of reproductive tactics in lubber grasshoppers. Oecologia, 132, 517–523.CrossRefGoogle Scholar
  24. Honek, A. (1993). Intraspecific variation in body size and fecundity in insects: A general relationship. Oikos, 66, 483–492.CrossRefGoogle Scholar
  25. Johnston, I. A., & Bennett, A. F. (1996). Animals and temperature: Phenotypic and evolutionary adaptation. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  26. Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.CrossRefGoogle Scholar
  27. Kingsolver, J. G., Hoekstra, H. E., Hoekstra, J. M., Berrigan, D., Vignieri, S. N., Hill, C. E., et al. (2001). The strength of phenotypic selection in natural populations. American Naturalist, 157, 245–261.CrossRefPubMedGoogle Scholar
  28. Kingsolver, J. G., & Huey, R. B. (2008). Size, temperature, and fitness: Three rules. Evolutionary Ecology Research, 10, 251.Google Scholar
  29. Kluen, E., de Heij, M. E., & Brommer, J. E. (2011). Adjusting the timing of hatching to changing environmental conditions has fitness costs in blue tits. Behavioral Ecology and Sociobiology, 65, 2091–2103.CrossRefGoogle Scholar
  30. Körner, C. (2003). Alpine plant life: Functional plant ecology of high mountain ecosystems. Berlin: Springer.CrossRefGoogle Scholar
  31. Laiolo, P., Illera, J. C., Melendez, L., Segura, A., & Obeso, J. R. (2015). Abiotic, biotic and evolutionary control of the distribution of C and N isotopes in food webs. American Naturalist, 185, 169–182.CrossRefPubMedGoogle Scholar
  32. Laiolo, P., Illera, J. C., & Obeso, J. R. (2013). Local climate determines intra- and interspecific variation in sexual size dimorphism in mountain grasshopper communities. Journal of Evolutionary Biology, 26, 2171–2183.CrossRefPubMedGoogle Scholar
  33. Laiolo, P., & Obeso, J. R. (2012). Multilevel selection and neighbourhood effects from individual to metapopulation in a wild passerine. PLoS ONE, 7(6), e38526.PubMedCentralCrossRefPubMedGoogle Scholar
  34. Lande, R., & Arnold, S. J. (1983). The measurement of selection on related characters. Evolution, 37, 1210–1226.CrossRefGoogle Scholar
  35. Laugen, A. T., 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.CrossRefPubMedGoogle Scholar
  36. Levinton, J. S. (1983). The latitudinal compensation hypothesis: Growth data and a model of latitudinal growth differentiation based upon energy budgets. I. Interspecific comparison of Ophryotrocha puerilis (Polychaeta: Dorvilleidae). Biological Bulletin, 165, 686–698.CrossRefGoogle Scholar
  37. Li, B., Suzuki, J. I., & Hara, T. (1998). Latitudinal variation in plant size and relative growth rate in Arabidopsis thaliana. Oecologia, 115, 293–301.CrossRefGoogle Scholar
  38. Lusk, C. H., Reich, P. B., Montgomery, R. A., Ackerly, D. D., & Cavender-Bares, G. (2008). Why are evergreen leaves so contrary about shade? Trends in Ecology & Evolution, 23, 299–303.CrossRefGoogle Scholar
  39. Parsons, S. M., & Joern, A. (2014). Life history traits associated with body size covary along a latitudinal gradient in a generalist grasshopper. Oecologia, 174, 379–391.CrossRefPubMedGoogle Scholar
  40. R Development Core Team. (2015). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. ISBN 3-900051-07-0. http://www.R-project.org.
  41. Roff, D. A. (2002). Life history evolution. Sunderland, MA: Sinauer Associates.Google Scholar
  42. Rotvit, L., & Jacobsen, D. (2014). Egg development of Plecoptera, Ephemeroptera and Odonata along latitudinal gradients. Ecological Entomology, 39, 177–185.CrossRefGoogle Scholar
  43. Samietz, F., Salser, M. A., & Dingle, H. (2005). Altitudinal variation in behavioural thermoregulation: Local adaptation vs. plasticity in California grasshoppers. Journal of Evolutionary Biology, 18, 1087–1096.CrossRefPubMedGoogle Scholar
  44. Santamaría, L., Figuerola, J., Pilon, J. J., Mjelde, M., Green, A. J., De Boer, T., et al. (2003). Plant performance across latitude: The role of plasticity and local adaptation in an aquatic plant. Ecology, 84, 2454–2461.CrossRefGoogle Scholar
  45. Santos, M., Fowler, K., & Partridge, L. (1994). Gene–environment interaction for body size and larval density in Drosophila melanogaster: An investigation of effects on development time, thorax length and adult sex ratio. Heredity, 72, 515–521.CrossRefPubMedGoogle Scholar
  46. Skelly, D. K. (2004). Microgeographic countergradient variation in the wood frog, Rana sylvatica. Evolution, 58, 160–165.CrossRefPubMedGoogle Scholar
  47. Sømme, L. (1989). Adaptations of terrestrial arthropods to the alpine environment. Biological Reviews, 64, 367–407.CrossRefGoogle Scholar
  48. Taylor, B. W., Anderson, C. R., & Peckarsky, B. L. (1998). Effects of size at metamorphosis on stonefly fecundity, longevity, and reproductive success. Oecologia, 114, 494–502.CrossRefGoogle Scholar
  49. Telfer, M. G., & Hassall, M. (1999). Ecotypic differentiation in the grasshopper Chorthippus brunneus: Life history varies in relation to climate. Oecologia, 121, 245–254.CrossRefGoogle Scholar
  50. Toräng, P., Wunder, J., Obeso, J. R., Herzog, M., Coupland, G., & Ågren, J. (2015). Large-scale adaptive differentiation in the alpine perennial herb Arabis alpina. New Phythologist, 206, 459–470.CrossRefGoogle Scholar
  51. Van Wingerden, W. K. R. E., Musters, J. C. M., & Maaskamp, F. I. M. (1991). The influence of temperature on the duration of egg development in West European grasshoppers (Orthoptera: Acrididae). Oecologia, 87, 417–423.CrossRefGoogle Scholar
  52. Verberk, W. C., Siepel, H., & Hsselink, H. (2008). Life-history strategies in freshwater macroinvertebrates. Freshwater Biology, 53, 1722–1738.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Research Unit of Biodiversity (UO, CSIC, PA)Oviedo UniversityMieresSpain

Personalised recommendations