Divergence and ontogenetic coupling of larval behaviour and thermal reaction norms in three closely related butterflies

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1703, 2011, Pages 313-320

  Berger, David ^a,b   Friberg, Magne ^a   Gotthard, Karl ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Co adaptation; Developmental plasticity; Environmental tolerance; Ontogeny; Performance curve; Temperature

Indexed keywords

BUTTERFLY; COEVOLUTION; EVOLUTIONARILY STABLE STRATEGY; FORAGING BEHAVIOR; GENERALIST; GROWTH RATE; ONTOGENY; PERFORMANCE ASSESSMENT; SPECIALIST; TEMPERATURE TOLERANCE; TRADE-OFF;

PAPILIONOIDEA;

EID: 78650493046     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1398     Document Type: Conference Paper

References (66)

1. Schmalhausen, I. I. 1949 Factors of evolution.Philadelphia, PA: Blakiston U.S.
2. Waddington, C. H. 1953 Genetic assimilation of an acquired character. Evolution 7, 118-126. (doi:10.2307/2405747)
3. Via, S. & Lande, R. 1985 Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505-522. (doi:10.2307/2408649)
4. Lande, R. 2009 Adaptation to an extraordinary environment by phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435-1446. (doi:10.1111/j.1420-9101.2009.01754.x)
5. Levins, R. 1968 Evolution in changing environments. Princeton, NJ: Princeton University Press.
6. Lynch, M. & Gabriel, W. 1987 Environmental tolerance. Am. Nat. 129, 283-303. (doi:10.1086/284635)
7. Gilchrist, G. W. 1995 Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. Am. Nat. 146, 252-270. (doi:10.1086/285797) (Pubitemid 26450753)
8. Arendt, J. D. 1997 Adaptive intrinsic growth rates: an integration across taxa. Q. Rev. Biol. 72, 149-177. (doi:10.1086/419764)
9. Angilletta, M. J., Wilson, R. S., Navas, C. A. & James, R. S. 2003 Tradeoffs and the evolution of thermal reaction norms. Trends Ecol. Evol. 18, 234-240. (doi:10.1016/S0169-5347(03)00087-9) (Pubitemid 36551228)
10. Angilletta, M. J., Bennett, A. F., Guderley, H., Navas, C. A., Seebacher, F. & Wilson, R. S. 2006 Coadaptation: a unifying principle in evolutionary thermal biology. Physiol. Biochem. Zool. 79, 282-294.
11. Dunbar, R. I., Korstjens, A. H. & Lehmann, J. 2009 Time as an ecological constraint. Biol. Rev. 84, 413-429. (doi:10.1111/j.1469-185X.2009. 00080.x)
12. Yamahira, K., Kawajiri, M., Takeshi, K. & Irie, T. 2007 Inter- and intrapopulation variation in thermal reaction norms for growth rate: evolution of latitudinal compensation in ectotherms with a genetic constraint. Evolution 61, 1577-1589. (doi:10.1111/j.1558-5646.2007.00130.x) (Pubitemid 47013465)
13. Huey, R. B. & Kingsolver, J. G. 1989 Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4, 131-135. (doi:10.1016/0169- 5347(89)90211-5)
14. Bennett, A. F. & Lenski, R. E. 1993 Evolutionary adaptation to temperature II. Thermal niches of experimental lines of Escherichia coli. Evolution 47, 1-12. (doi:10.2307/2410113)
15. Bennett, A. F. & Lenski, R. E. 2007 An experimental test of evolutionary trade-offs during temperature adaptation. Proc. Natl Acad. Sci. USA 104, 8649-8654. (doi:10.1073/pnas.0702117104) (Pubitemid 47175459)
16. Angilletta, M. J. 2009 Thermal adaptation - a theoretical and empirical synthesis. New York, NY: Oxford University Press.
17. Hochachka, P. W. & Somero, G. N. 2002 Biochemical adaptation: mechanism and process in physiological evolution. Oxford, UK: Oxford University Press.
18. Brett, J. R. 1971 Energetic responses of salmon to temperature. A study of some thermal relations in the physiology and freshwater ecology of sockeye salmon (Oncorhynchus nerka). Am. Zool. 11, 99-113.
19. Conover, D. O. & Schultz, E. T. 1995 Phenotypic similarity and the evolutionary significance of countergradient variation. Trends Ecol. Evol. 10, 248-252. (doi:10.1016/S0169-5347(00)89081-3)
20. Gotthard, K., Nylin, S. & Wiklund, C. 2000 Individual state controls temperature dependence in a butterfly (Lasiommata maera). Proc. R. Soc. Lond. B 267, 589593. (doi:10.1098/rspb.2000.1042)
21. Billerbeck, J. M., Lankford, T. E. & Conover, D. O. 2001 Evolution of intrinsic growth and energy acquisition rates. I. Trade-offs with swimming performance in Menidia menidia. Evolution 55, 1863-1872.
22. Lankford, T. E., Billerbeck, J. M. & Conover, D. O. 2001 Evolution of intrinsic growth and evergy acquisition rates. II. Trade-offs with vulnerability to predation in Menidia menidia. Evolution 55, 1873-1881. (doi:10.1111/j.0014-3820.2001.tb00836.x)
23. Gabriel, W. & Lynch, M. 1992 The selective advantage of reaction norms for environmental tolerance. J. Evol. Biol. 5, 41-59. (doi:10.1046/j.1420- 9101.1992.5010041.x)
24. Leroi, A. M., Bennett, A. F. & Lenski, R. E. 1994 Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc. Natl Acad. Sci. USA 91, 1917-1921. (doi:10.1073/pnas.91.5.1917)
25. Hoffmann, A. A. 1995 Acclimation: increasing survival at a cost. Trends Ecol. Evol. 10,1-2.
26. Bennett, A. F. & Lenski, R. E. 1997 Evolutionary adaptation to temperature. VI. Phenotypic acclimation and its evolution in Escherichia coli. Evolution 51, 36-44. (doi:10.2307/2410958)
27. Wilson, R. S. & Franklin, C. E. 2002 Testing the beneficial acclimation hypothesis. Trends Ecol. Evol. 17, 66-70. (doi:10.1016/S0169- 5347(01)02384-9) (Pubitemid 34142586)
28. Gabriel, W. 2005 How stress selects for reversible phenotypic plasticity. J. Evol. Biol. 18, 873-883. (doi:10.1111/j.1420-9101.2005.00959.x) (Pubitemid 40968540)
29. Kristensen, T. N., Hoffman, A. A., Overgaard, J., Sörensen, J. G., Hallas, R. & Loeschcke, V. 2008 Costs and benefits of cold acclimation in field-released Drosophila. Proc. Natl Acad. Sci. USA 105, 216-221. (doi:10.1073/pnas.0708074105)
30. Johnston, I. A., Viera, V. L. A. & Hill, J. 1996 Temperature and ontogeny in ectotherms: muscle phenotype in fish. In Animals and temperature (eds I. A. Johnston & A. F. Bennett), pp. 153-181. Cambridge, UK: Cambridge University Press.
31. Bowler, K. & Terblanche, J. S. 2008 Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol. Rev. 83, 339-355. (doi:10.1111/j.1469-185X.2008.00046.x) (Pubitemid 352020260)
32. Kozlowski, J. 1992 Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol. Evol. 7, 15-19. (doi:10.1016/0169-5347(92)90192-E)
33. Roff, D. A. 2002 Life history evolution. Sunderland, MA: Sinnauer Associates Inc.
34. Lima, S. L. & Dill, L. M. 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640. (doi:10.1139/z90-092)
35. Werner, E. E. & Gilliam, J. F. 1984 The ontogenetic niche and species interactions in size-structured populations. Ann. Rev. Ecol. Syst. 15, 393-425. (doi:10.1146/annurev.es.15.110184.002141)
36. Kronfeld-Schor, N. & Dayan, T. 2003 Partitioning of time as an ecological resource. Ann. Rev. Ecol. Evol. Syst. 34, 153-181. (doi:10.1146/annurev.ecolsys.34.011802.132435)
37. West-Eberhard, M. 2003 Developmental plasticity and evolution. New York, NY: Oxford University press.
38. Zani, P. A., Cohnstaedt, L. W., Corbin, D., Bradshaw, W. E. & Holzapfel, C. M. 2005 Reproductive value in a complex life cycle: heat tolerance of the pitcher-plant mosquito, Wyeomyia smithii. J. Evol. Biol. 18, 101-105. (doi:10.1111/j.1420-9101.2004.00793.x)
39. Berger, D., Walters, R. & Gotthard, K. 2006 What keeps insects small? Size dependent predation on two species of butterfly larvae. Evol. Ecol. 20, 575-589. (doi:10.1007/s10682-006-9118-8) (Pubitemid 44701112)
40. Berger, D. & Gotthard, K. 2008 Time stress, predation risk and diurnal-nocturnal foraging trade offs in larval prey. Behav. Ecol. Soc. 62, 1655-1663. (doi:10.1007/s00265-008-0594-4)
41. Tolman, T. 1997 Butterflies of Europe. Princeton, NJ: Princeton University Press.
42. Weingartner, E., Wahlberg, N. & Nylin, S. 2006 Speciation in Pararge (Satyrinae: Nymphalidae) butterflies - North Africa is the source of ancestral populations of all Pararge species. Syst. Entomol. 31 , 621-632. (doi:10.1111/j.1365-3113.2006.00333.x) (Pubitemid 44527172)
43. Gotthard, K., Berger, D., Bergman, M. & Merilaita, S. 2009 The evolution of alternative morphs: density-dependent determination of larval colour dimorphism in a butterfly. Biol. J. Linn. Soc. 98, 256-266. (doi:10.1111/j.1095-8312.2009.01290.x)
44. R Development Core Team. 2007 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
45. Stevenson, R. D. 1985 The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. Am. Nat. 126, 362-386. (doi:10.1086/284423)
46. Casey, T. M. 1976 Activity patterns, body temperature and thermal ecology in two desert caterpillars (Lepidoptera: Sphingidae). Ecology 57, 485-497. (doi:10.2307/1936433)
47. Kingsolver, J. G. 2000 Feeding, growth, and the thermal environment of cabbage white caterpillars, Pieris rapae L. Physiol. Biochem. Zool. 73,621-628.(doi:10.1086/317758) (Pubitemid 32044980)
48. Gotthard, K., Berger, D. & Walters, R. J. 2007 What keeps insects small? Time limitation during oviposition reduces the fecundity benefit of female size in a butterfly. Am. Nat. 169, 768-779. (doi:10.1086/516651) (Pubitemid 46847332)
49. Kingsolver, J. G., Gomulkiewicz, R. & Carter, P. A. 2001 Variation, selection and evolution of function valued traits. Genetica 112-113, 87-104. (doi:10.1023/A:1013323318612) (Pubitemid 34119655)
50. Gomulkiewicz, R. & Kirkpatrick, M. 1992 Quantitative genetics and the evolution of reaction norms. Evolution 46, 390-411. (doi:10.2307/2409860)
51. Martin, T. L. & Huey, R. B. 2008 Why 'suboptimal' is optimal: Jensens's inequality and ectotherm thermal preference. Am. Nat. 171, E102-E118. (doi:10.1086/527502) (Pubitemid 351358632)
52. Frazier, M. R., Huey, R. B. & Berrigan, D. 2006 Thermodynamics constrain the evolution of insect population growth rates: 'warmer is better'. Am. Nat. 168, 512-520. (doi:10.1086/506977) (Pubitemid 44582857)
53. Asbury, D. A. & Angilletta, M. J. 2010 Thermodynamic effects on the evolution of performance curves. Am. Nat. 176, E40-E49. (doi:10.1086/653659)
54. Knies, J. L., Kingsolver, J. G. & Burch, C. L. 2009 Hotter is better and broader: thermal sensitivity of fitness in a population of bacteriophages. Am. Nat. 173, 419-430. (doi:10.1086/597224)
55. Kingsolver, J. G. & Gomulkiewicz, R. 2003 Environmental variation and selection on performance curves. Integr. Comp. Biol. 43, 470-477.(doi:10.1093/ icb/43.3.470)
56. Huey,R.B., Hertz, P. E. & Sinervo,B.2003 Behavioral drive versus behavioral inertia in evolution: a null model approach. Am. Nat. 161, 357-366. (doi:10.1086/346135) (Pubitemid 36391912)
57. Huey, R. B. & Bennett, A. F. 1987 Phylogenetic studies of coadaptation: preferred temperatures versus optimal performance temperatures of lizards. Evolution 41, 1098-1115. (doi:10.2307/2409194)
58. Casey, T. M. 1993 Effects of temperature on foraging in caterpillars. In Caterpillars - ecological and evolutionary constraints on foraging (eds N. E. Stamp & T. M. Casey), pp. 5-28. New York, NY: Chapman & Hall.
59. Stamp, N. E. & Wilkens, R. T. 1993 On the cryptic side of lite: being unapparent to enemies and the consequences for foraging and growth in caterpillars. In Caterpillars - ecological and evolutionary constraints on foraging (eds N. E. Stamp & T. M. Casey), pp. 283-330. New York, NY: Chapman & Hall.
60. Stamp, N. E. & Bowers, D. 1993 Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71, 1031-1039. (doi:10.2307/1937371)
61. Huey, R. B. & Slatkin, M. 1976 Cost and benefits of lizard thermoregulation. Q. Rev. Biol. 51, 363-384. (doi:10.1086/409470)
62. Izem, R. & Kingsolver, J. G. 2005 Variation in continuous reaction norms: quantifying directions of biological interest. Am. Nat. 166, 277-289. (doi:10.1086/431314) (Pubitemid 41076650)
63. Chown, S. L., Jumbam, K. R., Sörensen, J. G. & Terblanche, J. S. 2009 Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct. Ecol. 23, 133-140. (doi:10.1111/j.1365-2435.2008.01481.x)
64. Lynch, M. & Walsh, B. 1998 Genetics and analysis of quantitative traits. Sunderland, MA: Sinauer Associates Inc.
65. Hoffmann, A. A. & Merilä, J. 1999 Heritable variation and evolution under favourable and unfavourable conitions. Trends Ecol. Evol. 14, 96-101. (doi:10.1016/S0169-5347(99)01595-5) (Pubitemid 29135081)
66. Scheiner, S. M. 1993 Genetics and evolution of phenotypic plasticity. Ann. Rev. Ecol. Syst. 24, 35-68. (doi:10.1146/annurev.es.24.110193.000343)