The impact of thermal fluctuations on reaction norms in specialist and generalist parasitic wasps

Functional Ecology

Volumn 28, Issue 2, 2014, Pages 411-423

  Foray, Vincent ^a,b   Desouhant, Emmanuel ^a   Gibert, Patricia ^a  

^a UNIVERSITÉ LYON 1   (France)

^b EARTH AND LIFE INSTITUTE   (Belgium)

Author keywords

Environmental variability; Jensen's Inequality; Parasitoid; Performance curves; Phenotypic plasticity; Venturia canescens

Indexed keywords

ENVIRONMENTAL EFFECT; FITNESS; GENE EXPRESSION; HOST-PARASITE INTERACTION; HOST-PARASITOID INTERACTION; LIFE HISTORY TRAIT; PHENOTYPE; PREDICTION; TEMPERATURE EFFECT; WASP;

VENTURIA CANESCENS; VESPOIDEA;

EID: 84896039181     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12171     Document Type: Article

References (83)

1. Addo-Bediako, A., Chown, S.L. & Gaston, K.J. (2002) Metabolic cold adaptation in insects: a large-scale perspective. Functional Ecology, 16, 332-338.
2. Amat, I. (2004) Coexistence de la reproduction sexuée et asexuée chez l'hyménoptère parasitoïde Venturia canescens: Aspects comportementaux et écologiques. PhD thesis, Université Claude Bernard Lyon 1, Lyon.
3. Amat, I., Desouhant, E. & Bernstein, C. (2009) Differential use of conspecific-derived information by sexual and asexual parasitic wasps exploiting partially depleted host patches. Behavioral Ecology and Sociobiology, 63, 563-572.
4. Amat, I., Castelo, M., Desouhant, E. & Bernstein, C. (2006) The influence of temperature and host availability on the host exploitation strategies of sexual and asexual parasitic wasps of the same species. Oecologia, 148, 153-161.
5. Angilletta, M.J. (2009) Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press, Oxford.
6. Beukeboom, L.W., Driessen, G., Luckerhoff, L., Bernstein, C., Lapchin, L. & Van Alphen, J.J.M. (1999) Distribution and relatedness of sexual and asexual Venturia canescens (Hymenoptera). Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society, 10, 23-28.
7. Blackburn, H.B., Hobbs, N.T. & Detling, J.K. (2011) Nonlinear responses to food availability shape effects of habitat fragmentation on consumers. Ecology, 92, 98-107.
8. Boggs, C.L. (1992) Resource allocation: exploring connections between foraging and life history. Functional Ecology, 6, 508-518.
9. Bolnick, D.I., Amarasekare, P., Araújo, M.S., Bürger, R., Levine, J.M., Novak, M. et al. (2011) Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution, 26, 183-192.
10. Bozinovic, F., Bastias, D.A., Boher, F., Clavijo-Baquet, S., Estay, S.A. & Angilletta, M.J. (2011) The mean and variance of environmental temperature interact to determine physiological tolerance and fitness. Physiological and Biochemical Zoology, 84, 543-552.
11. Brakefield, P.M. & Kesbeke, F. (1997) Genotype-environment interactions for insect growth in constant and fluctuating temperature regimes. Proceedings of the Royal Society of London. Series B, Biological Sciences, 264, 717-723.
12. Brommer, J.E., Rattiste, K. & Wilson, A.J. (2008) Exploring plasticity in the wild: laying date-temperature reaction norms in the common gull Larus canus. Proceeding of the Royal Society B: Biological Sciences, 275, 687-693.
13. Caraco, T. (1980) On foraging time allocation in a stochastic environment. Ecology, 61, 119-128.
14. Castelo, M.K., Corley, J.C. & Desouhant, E. (2003) Conspecific avoidance during foraging in Venturia canescens (Hymenoptera: Ichneumonidae): the roles of host presence and conspecific densities. Journal of Insect Behavior, 16, 307-318.
15. Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Kruuk, L.E.B. & Sheldon, B.C. (2008) Adaptive Phenotypic Plasticity in Response to Climate Change in a Wild Bird Population. Science, 320, 800-803.
16. Chevin, L.M., Lande, R. & Mace, G.M. (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biology, 8, e1000357.
17. Chown, S.L., Slabber, S., McGeoch, M.A., Janion, C. & Leinaas, H.P. (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proceedings of the Royal Society of London. Series B, Biological Sciences, 274, 2531-2537.
18. Chown, S.L., Hoffmann, A.A., Kristensen, T.N., Anguilletta, M.J., Nils, C.S. & Pertoldi, C. (2010) Adapting to climate change: a perspective from evolutionary physiology. Climate Research, 43, 3-15.
19. Clarke, A. (1993) Seasonal acclimatization and latitudinal compensation in metabolism: do they exist? Functional Ecology, 7, 139-149.
20. Clusella-Trullas, S., Blackburn, T.M. & Chown, S.L. (2011) Climatic predictors of temperature performance curve parameters in ectotherms imply complex responses to climate change. American Naturalist, 177, 738-751.
21. Colinet, H., Hance, T., Vernon, P., Bouchereau, A. & Renault, D. (2007) Does fluctuating thermal regime trigger free amino acid production in the parasitic wasp Aphidius colemani (Hymenoptera: Aphidiinae). Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology, 147, 484-492.
22. Desouhant, E., Driessen, G., Amat, I. & Bernstein, C. (2005) Host and food searching in a parasitic wasp Venturia canescens: a trade-off between current and future reproduction? Animal Behavior, 70, 145-152.
23. Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl, T.R. & Mearns, L.O. (2000) Climate extremes: observations, modeling, and impacts. Science, 289, 2068-2074.
24. Eliopoulos, P.A. & Stathas, G.J. (2003) Temperature-Dependent Development of the Koinobiont Endoparasitoid Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae): Effect of host instar. Environmental Entomology, 32, 1049-1055.
25. Eliopoulos, P.A., Harvey, J.A., Athanassiou, G. & Stathas, G.J. (2003) Effect of biotic and abiotic factors on reproductive parameters of the synovigenic endoparasitoid Venturia canescens. Physiological Entomology, 28, 268-275.
26. Ellers, J. & van Alphen, J.J.M. (1997) Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction. Journal of Evolutionary Biology, 10, 771-785.
27. Ernande, B. & Dieckmann, U. (2004) The evolution of phenotypic plasticity in spatially structured environments: implications of intraspecific competition, plasticity costs and environmental characteristics. Journal of Evolutionary Biology, 17, 613-628.
28. Fischer, B., Dieckmann, U. & Taborsky, B. (2011) When to store energy in a stochastic environment. Evolution, 65, 1221-1232.
29. Fischer, B., Taborsky, B. & Dieckmann, U. (2009) Unexpected patterns of plastic energy allocation in stochastic environments. American Naturalist, 173, 108-120.
30. Fischer, K., Kölzow, N., Höltje, H. & Karl, I. (2011) Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia, 166, 23-33.
31. Folguera, G., Bastias, D.A., Caers, J., Rojas, J.M., Piulachs, M.-D., Bellès, X. et al. (2011) An experimental test of the role of environmental temperature variability on ectotherm molecular, physiological and life-history traits: implications for global warming. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Biology, 159, 242-246.
32. Foray, V., Gibert, P. & Desouhant, E. (2011) Differential thermal performance curves in response to different habitats in the parasitoid Venturia canescens. Naturwissenschaften, 98, 683-691.
33. Foray, V., Pélisson, P.F., Bel-Venner, M.C., Desouhant, E., Venner, S., Menu, F. et al. (2012) A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited. Physiological Entomology, 37, 295-302.
34. Foray, V., Henri, H., Martinez, S., Gibert, P. & Desouhant, E. (2013a) Occurrence of arrhenotoky and thelytoky in a parasitic wasp Venturia canescens (Hymenoptera: Ichneumonidae): effect of endosymbionts or existence of two distinct reproductive modes? European Journal of Entomology, 110, 103-107.
35. Foray, V., Desouhant, E., Voituron, Y., Larvor, V., Renault, D., Colinet, H. et al. (2013b) Does cold tolerance plasticity correlate with the thermal environment and metabolic profiles of a parasitoid wasp?. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 164, 77-83.
36. Gilchrist, G.W. (1995) Specialists and Generalists in Changing Environments. I. Fitness Landscapes of Thermal Sensitivity. American Naturalist, 146, 252-270.
37. Hance, T., van Baaren, J., Vernon, P. & Boivin, G. (2007) Impact of Extreme Temperature on Parasitoids in a Climate Change Perspective. Annual Review of Entomology, 52, 107-126.
38. van Handel, E. (1985a) Rapid determination of glycogen and sugars in mosquitoes. Journal of American Mosquitoes Control Association, 1, 299-301.
39. van Handel, E. (1985b) Rapid determination of total lipids in mosquitoes. Journal of American Mosquitoes Control Association, 1, 302-304.
40. Huey, R.B. & Stevenson, R. (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. American Zoologist, 19, 357-366.
41. Jensen, J.L. (1906) Sur les fonctions convexes et les inégualités entre les valeurs moyennes. Acta Mathematica, 30, 175-193.
42. Kingsolver, J.G., Ragland, G.J. & Diamond, S.E. (2009) Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of Manduca sexta. Evolution, 63, 537-541.
43. Kjærsgaard, A., Le, N., Demontis, D., Novicic, Z.K., Loeschcke, V. & Pertoldi, C. (2012) The effect of developmental temperature fluctuation on wing traits and stressed locomotor performance in Drosophila melanogaster, and its dependence. Evolutionary Ecology Research, 14, 803-819.
44. Koštál, V., Renault, D., Mehrabianova, A. & Bastl, J. (2007) Insect cold tolerance and repair of chill-injury at fluctuating thermal regimes: role of ion homeostasis. Comparative Biochemistry and Physiology. Part A, Molecular and Integrative Physiology, 147, 231-238.
45. Li, H. & Reynolds, J.F. (1993) A new contagion index to quantify spatial patterns of landscapes. Landscape Ecology, 8, 155-162.
46. Liu, Y.Q., Bernstein, C. & Thiel, A. (2009b) Travel duration, energetic expenditure, and patch exploitation in the parasitic wasp Venturia canescens. Behavioral Ecology and Sociobiology, 63, 1459-1469.
47. Liu, Y.Q., Thiel, A. & Hoffmeister, T.S. (2009a) Odor-mediated patch choice in the parasitoid Venturia canescens: temporal decision dynamics. Entomologia Experimentalis et Applicata, 132, 110-117.
48. Lucchetta, P., Desouhant, E., Wajnberg, E. & Bernstein, C. (2007) Small but smart: the interaction between environmental cues and internal state modulates host-patch exploitation in a parasitic wasp. Behavioral Ecology and Sociobiology, 61, 1409-1418.
49. Lynch, M. & Gabriel, W. (1987) Environmental Tolerance. American Naturalist, 129, 283-303.
50. Marshall, K.E. & Sinclair, B.J. (2010) Repeated stress exposure results in a survival-reproduction trade-off in Drosophila melanogaster. Proceedings of the Royal Society of London. Series B, Biological Sciences, 277, 963-969.
51. Martin, T.L. & Huey, R.B. (2008) Why "suboptimal" is optimal: Jensen's Inequality and ectotherm thermal preferences. American Naturalist, 171, e102-118.
52. Mateo-Leach, I., Hesseling, A., Huibers, W., Witsenboer, H., Beukeboom, L. & Van De Zande, L. (2009) Transcriptome and proteome analysis of ovaries of arrhenotokous and thelytokous Venturia canescens. Insect Molecular Biology, 18, 477-482.
53. Měráková, E. & Goždík, L. (2009) Thermal acclimation of swimming performance in newt larvae: the influence of diel temperature fluctuations during embryogenesis. Functional Ecology, 23, 989-995.
54. Metzger, M., Bernstein, C. & Desouhant, E. (2008) Does constrained oviposition influence offspring sex ratio in the solitary parasitoid wasp Venturia canescens? Ecological Entomology, 33, 167-174.
55. Miner, B.G. & Vonesh, J.R. (2004) Effects of fine grain environmental variability on morphological plasticity. Ecology Letters, 7, 794-801.
56. Moran, N.A. (1992) The evolutionary maintenance of alternative phenotypes. American Naturalist, 139, 971-989.
57. Nelder, J.A. & Weddenburn, R.W.M. (1972) Generalized linear models. Journal of the Royal Statistical Society. Series A, 135, 370-384.
58. Niehaus, A.C., Angilletta, M.J., Sears, M.W., Franklin, C.E. & Wilson, R.S. (2012) Predicting the physiological performance of ectotherms in fluctuating thermal environments. The Journal of Experimental Biology, 215, 694-701.
59. Pasztor, L., Kisdi, E. & Meszena, G. (2000) Jensen's inequality and optimal life history strategies in stochastic environments. Trends in Ecology & Evolution, 15, 117-118.
60. Pelosse, P., Bernstein, C. & Desouhant, E. (2007) Differential energy allocation as an adaptation to different habitats in the parasitic wasp Venturia canescens. Evolutionary Ecology, 21, 669-685.
61. Pelosse, P., Amat, I., Bernstein, C. & Desouhant, E. (2010) The dynamics of energy allocation in adult arrhenotokous and thelytokous Venturia canescens. Entomologia Experimentalis et Applicata, 135, 68-76.
62. Pelosse, P., Jervis, M.A., Bernstein, C. & Desouhant, E. (2011) Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness? Biological Journal of the Linnean Society, 104, 621-632.
63. Pétavy, G., David, J.R., Gibert, P. & Moreteau, B. (2001) Viability and rate of development at different temperatures in Drosophila: a comparison of constant and alternating regimes. Journal of Thermal Biology, 26, 29-39.
64. Pétavy, G., David, J.R., Debat, V., Gibert, P. & Moreteau, B. (2004) Specific effects of cycling stressful temperatures upon phenotypic and genetic variability of size traits in Drosophila melanogaster. Evolutionary Ecology Research, 6, 873-890.
65. Podrabsky, J.E. & Somero, G.N. (2004) Changes in gene expression associated with acclimation to constant temperatures and fluctuating daily temperatures in an annual killifish Austrofundulus limnaeus. Journal of Experimental Biology, 207, 2237-2254.
66. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
67. Ragland, G.J. & Kingsolver, J.G. (2008) The effect of fluctuating temperatures on ectotherm life-history traits: comparisons among geographic populations of Wyeomyia smithii. Evolutionary Ecology Research, 10, 29-44.
68. Richards, S.A., Williams, N.M. & Harder, L.D. (2009) Variation in pollination: causes and consequences for plant reproduction. American Naturalist, 174, 382-398.
69. Rohr, J.R., Dobson, A.P., Johnson, P.T.J., Kilpatrick, A.M., Paull, S.H., Raffel, T.R. et al. (2011) Frontiers in climate change-disease research. Trends in Ecology & Evolution, 26, 270-277.
70. Ruel, J.J. & Ayres, M.P. (1999) Jensen's Inequality predicts effects of environmental variation. Trends in Ecology and Evolution, 14, 361-366.
71. Salt, G. (1976) The hosts of Nemeritis canescens, a problem in the host specificity of insect parasitoids. Ecological Entomology, 1, 63-67.
72. Schneider, M.V. (2003) Modes of reproduction in the solitary parasitoid wasp Venturia canescens. PhD thesis, Leiden University, the Netherlands.
73. Smallwood, P.D. (1996) An introduction to risk sensitivity: the use of Jensen's Inequality to clarify evolutionary arguments of adaptation and constraint. American Zoologist, 36, 392-317.
74. Stearns, S.C. (1976) Life-history tactics: a review of the ideas. Quaterly Review of Biology, 51, 3-46.
75. Stearns, S.C. (1989) Trade-offs in life-history evolution. Functional Ecology, 3, 259-268.
76. Tebaldi, C., Hayhoe, K., Arblaster, J.M. & Meehl, G.A. (2006) Going to the extremes: an intercomparison of model-simulated historical and future changes in extreme events. Climatic Change, 79, 185-211.
77. Terblanche, J.S., Nyamukondiwa, C. & Kleynhans, E. (2010) Thermal variability alters climatic stress resistance and plastic responses in a globally invasive pest, the Mediterranean fruit fly (Ceratitis capitata). Entomologia Experimentalis et Applicata, 137, 304-315.
78. Thiel, A., Driessen, G. & Hoffmeister, T.S. (2006) Different habitats, different habits? Response to foraging information in the parasitic wasp Venturia canescens. Behavioral Ecology and Sociobiology, 59, 614-623.
79. van Tienderen, P.H. (1991) Evolution of generalists and specialist in spatially heterogeneous environments. Evolution, 45, 1317-1331.
80. West-Eberhard, M.J. (2003) Developmental Plasticity and Evolution. Oxford University Press, New York.
81. Williams, C.M., Marshall, K.E., MacMillan, H.A., Dzurisin, J.D.K., Hellmann, J.J. & Sinclair, B.J. (2012) Thermal variability increases the impact of autumnal warming and drives metabolic depression in an overwintering butterfly. PLoS ONE, 7, e34470.
82. Wolf, M. & Weissing, F.J. (2012) Animal personalities: consequences for ecology and evolution. Trends in Ecology & Evolution, 27, 452-461.
83. Zhou, L., Dai, A., Vose, R.S., Zou, C., Tian, Y. & Chen, H. (2009) Spatial dependence of diurnal temperature range trends on precipitation from 1950 to 2004. Climate Dynamics, 32, 429-440.