Effects of temperature on reproductive output, egg provisioning, juvenile hormone and vitellogenin titres in the butterfly Bicyclus anynana

Journal of Insect Physiology

Volumn 54, Issue 8, 2008, Pages 1253-1260

  Geister, Thorin L ^a   Lorenz, Matthias W ^a   Meyering Vos, Martina ^a   Hoffmann, Klaus H ^a   Fischer, Klaus ^a,b  

^a UNIVERSITY OF BAYREUTH   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Egg composition; Egg size; Fecundity; Hormonal control; Insect; Phenotypic plasticity; Reproductive investment

Indexed keywords

BICYCLUS ANYNANA; HEXAPODA; PAPILIONOIDEA;

EID: 77950298396     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2008.06.002     Document Type: Article

References (84)

1. Atkinson D. Temperature and organism size-a biological law for ectotherms?. Advances in Ecological Research 1994, 25:1-58.
2. Avelar T. Egg size in Drosophila - standard-unit of investment or variable response to environment - the effect of temperature. Journal of Insect Physiology 1993, 39:283-289.
3. Azevedo R.B.R., French V., Partridge L. Life-history consequences of egg size in Drosophila melanogaster. American Naturalist 1997, 150:250-282.
4. Bauerfeind S.S., Fischer K. Effects of adult-derived carbohydrates, amino acids and micronutrients on female reproduction in a fruit-feeding butterfly. Journal of Insect Physiology 2005, 51:545-554.
5. Beenakkers A.M.T., Van der Horst D.J., Van Marrewijk W.J.A. Insect lipids and lipoproteins, and their role in physiological processes. Progress in Lipid Research 1985, 24:19-67.
6. Bernardo J. The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. American Zoologist 1996, 36:216-236.
7. Blanckenhorn W.U. Temperature effects on egg size and their fitness consequences in the yellow dung fly Scathophaga stercoraria. Evolutionary Ecology 2000, 14:627-643.
8. Braby M.F., Jones R.E. Reproductive patterns and resource-allocation in tropical butterflies-influence of adult diet and seasonal phenotype on fecundity, longevity and egg size. Oikos 1995, 72:189-204.
9. Bradshaw A.D. Phenotypic plasticity in plants. Advances in Genetics 1965, 13:115-155.
10. Brakefield P.M. Phenotypic plasticity and fluctuating asymmetry as responses to environmental stress in the butterfly Bicyclus anynana. Environmental Stress: Adaption and Evolution 1997, 65-67. Birkhäuser, Basel. R.R. Bijlsma, V. Loeschcke (Eds.).
11. Brakefield P.M., Kesbeke F., Koch P.B. The regulation of phenotypic plasticity of eyespots in the butterfly Bicyclus anynana. American Naturalist 1998, 152:853-860.
12. Caley M.J., Schwarzkopf L., Shine R. Does total reproductive effort evolve independently of offspring size?. Evolution 2001, 55:1245-1248.
13. Casas J., Pincebourde S., Mandon N., Vannier F., Poujol R., Giron D. Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 2005, 86:545-554.
14. Czesak M.E., Fox C.W. Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments. Evolution 2003, 57:1121-1132.
15. de Wilde J., Beetsma J. The physiology of caste development in social insects. Advances in Insect Physiology 1982, 16:167-246.
16. Dingle H., Winchell R. Juvenile hormone as a mediator of plasticity in insect life histories. Archives of Insect Biochemistry and Physiology 1997, 35:359-373.
17. Diss A.L., Kunkel J.G., Montgomery M.E., Leonard D.E. Effects of maternal nutrition and egg provisioning on parameters of larval hatch, survival and dispersal in the gypsy moth, Lymantria dispar L. Oecologia 1996, 106:470-477.
18. Einum S., Fleming I.A. Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 2000, 405:565-567.
19. Emlen D.J., Nijhout H.F. Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Journal of Insect Physiology 1999, 45:45-53.
20. Endler J.A. Natural Selection in the Wild 1986, Princeton University Press, Princeton, NJ.
21. Ernsting G., Isaaks A. Ectotherms, temperature, and trade-offs: size and number of eggs in a carabid beetle. American Naturalist 2000, 155:804-813.
22. Finch C.E., Rose M.R. Hormones and the physiological architecture of life-history evolution. Quarterly Review of Biology 1995, 70:1-52.
23. Fischer K. Control of reproduction and a survival cost to mating in female Bicyclus anynana butterflies. Ecological Entomology 2007, 32:674-681.
24. Fischer K., Bot A.N.M., Brakefield P.M., Zwaan B.J. Fitness consequences of temperature-mediated egg size plasticity in a butterfly. Functional Ecology 2003, 17:803-810.
25. Fischer K., Brakefield P.M., Zwaan B.J. Plasticity in butterfly egg size: why larger offspring at lower temperatures?. Ecology 2003, 84:3138-3147.
26. Fischer K., Eenhoorn E., Bot A.N.M., Brakefield P.M., Zwaan B.J. Cooler butterflies lay larger eggs: developmental plasticity versus acclimation. Proceedings of the Royal Society of London Series B-Biological Sciences 2003, 270:2051-2056.
27. Fischer K., O'Brien D.M., Boggs C.L. Allocation of larval and adult resources to reproduction in a fruit-feeding butterfly. Functional Ecology 2004, 18:656-663.
28. Fischer K., Bot A.N.M., Brakefield P.M., Zwaan B.J. Do mothers producing large offspring have to sacrifice fecundity?. Journal of Evolutionary Biology 2006, 19:380-391.
29. Flatt T., Kawecki T.J. Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster. Evolution 2007, 61:1980-1991.
30. Flatt T., Tu M.P., Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 2005, 27:999-1010.
31. Fox C., Czesak M. Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 2000, 45:341-369.
32. Gäde G., Hoffmann K.H., Spring J.H. Hormonal regulation in insects: facts, gaps, and future directions. Physiological Reviews 1997, 77:963-1032.
33. Ganong W. Lehrbuch der medizinischen Physiologie 1974, Springer, Berlin.
34. Geister T.L., Lorenz M.W., Hoffmann K.H., Fischer K. Effects of the NMDA receptor antagonist MK-801 on female reproduction and juvenile hormone biosynthesis in the cricket Gryllus bimaculatus and the butterfly Bicyclus anynana. Journal of Experimental Biology 2008, 211:1587-1593.
35. Ghalambor C.K., McKay J.K., Carroll S.P., Reznick D.N. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 2007, 21:394-407.
36. Gilbert L.I., Granger N.A., Roe R.M. The juvenile hormones: historical facts and speculations on future research directions. Insect Biochemistry and Molecular Biology 2000, 30:617-644.
37. Giron D., Casas J. Mothers reduce egg provisioning with age. Ecology Letters 2003, 6:273-277.
38. Gotthard K., Nylin S. Adaptive plasticity and plasticity as an adaption: a selective review of plasticity in animal morphology and life history. Oikos 1995, 74:3-17.
39. Hodin J., Riddiford L.M. Different mechanisms underlie phenotypic plasticity and interspecific variation for a reproductive character in drosophilids (Insecta: Diptera). Evolution 2000, 54:1638-1653.
40. Hoffmann K.H. Oogenesis and the female reproductive tract. Insect Reproduction 1995, 1-32. CRC Press, New York. J. Hardy, S.R. Leather (Eds.).
41. Huey R.B., Wakefield T., Crill W.D., Gilchrist G.W. Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster. Heredity 1995, 74:216-223.
42. Jaeckle W. Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development. Ecology of Marine Invertebrate Larvae 1995, 49-77. CRC Press, Boca Raton. L. McEdward (Ed.).
43. Jann P., Ward P.I. Maternal effects and their consequences for offspring fitness in the yellow dung fly. Functional Ecology 1999, 13:51-58.
44. Jarošík V., Kratochvil L., Honek A., Dixon A.F.G. A general rule for the dependence of developmental rate on temperature in ectothermic animals. Proceedings of the Royal Society of London Series B-Biological Sciences 2004, 271:S219-S221.
45. Jervis M.A., Ferns P.N. The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos 2004, 107:449-461.
46. Karl I., Lorenz M.W., Fischer K. Energetics of reproduction: consequences of divergent selection on egg size, food limitation, and female age for egg composition and reproductive effort in a butterfly. Biological Journal of the Linnean Society 2007, 91:403-418.
47. Karlsson B., Wiklund C. Egg weight variation and lack of correlation between egg weight and offspring fitness in the wall brown butterfly Lasiommata megera. Oikos 1984, 43:376-385.
48. Koch P.B., Brakefield P.M., Kesbeke F. Ecdysteroids control eyespot size and wing color pattern in the polyphenic butterfly Bicyclus anynana (Lepidoptera: Satyridae). Journal of Insect Physiology 1996, 42:223-230.
49. Kyneb A., Toft S. Effects of maternal diet quality on offspring performance in the rove beetle Tachyporus hypnorum. Ecological Entomology 2006, 31:322-330.
50. Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage T4. Nature 1970, 227:680-685.
51. Larsen T.B. The Butterflies of Kenya and Their Natural history 1991, Oxford University Press, Oxford, UK.
52. Levins R. Theory of fitness in a heterogeneous environment. II. Developmental flexibility and niche selection. American Naturalist 1963, 47:75-90.
53. Lorenz M.W. Adipokinetic hormone inhibits the formation of energy stores and egg production in the cricket Gryllus bimaculatus. Comparative Biochemistry and Physiology B 2003, 136:197-206.
54. McIntyre G.S., Gooding R.H. Egg size, contents, and quality: maternal-age and -size effects on house fly eggs. Canadian Journal of Zoology 2000, 78:1544-1551.
55. Miner B.G., Sultan S.E., Morgan S.G., Padilla D.K., Relyea R.A. Ecological consequences of phenotypic plasticity. Trends in Ecology and Evolution 2005, 20:685-692.
56. Nijhout H. Insect Hormones 1994, Princeton University Press, Princeton.
57. Nijhout H.F. Control mechanisms of polyphenic development in insects-in polyphenic development, environmental factors alter same aspects of development in an orderly and predictable way. Bioscience 1999, 49:181-192.
58. Nussey D.H., Wilson A.J., Brommer J.E. The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of Evolutionary Biology 2007, 20:831-844.
59. Pigliucci M. Evolution of phenotypic plasticity: where are we going now?. Trends in Ecology and Evolution 2005, 20:481-486.
60. Raikhel A.S., Dhadialla T.S. Accumulation of yolk proteins in insect oocytes. Annual Review of Entomology 1992, 37:217-251.
61. Ramaswamy S.B., Shu S.Q., Park Y.I., Zeng F.R. Dynamics of juvenile hormone-mediated gonadotropism in the Lepidoptera. Archives of Insect Biochemistry and Physiology 1997, 35:539-558.
62. Sappington T.W., Raikhel A.S. Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochemistry and Molecular Biology 1998, 28:277-300.
63. Schwarzkopf L., Blows M.W., Caley M.J. Life-history consequences of divergent selection on egg size in Drosophila melanogaster. American Naturalist 1999, 154:333-340.
64. Silbernagel S., Despopolos A. Taschenatlas der Physiologie 1991, Thieme, Stuttgart.
65. Sinervo B., Svensson E. Mechanistic and selective causes of life history trade-offs and plasticity. Oikos 1998, 83:432-442.
66. Smith C.C., Fretwell D.S. The optimal balance between size and number of offspring. American Naturalist 1974, 108:499-506.
67. Sorge D., Nauen R., Range S., Hoffmann K.H. Regulation of vitellogenesis in the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae). Journal of Insect Physiology 2000, 46:969-976.
68. Steigenga M.J., Fischer K. Ovarian dynamics, egg size, and egg number in relation to temperature and mating status in a butterfly. Entomologia Experimentalis et Applicata 2007, 125:195-203.
69. Steigenga M.J., Zwaan B.J., Brakefield P.M., Fischer K. The evolutionary genetics of egg size plasticity in a butterfly. Journal of Evolutionary Biology 2005, 18:281-289.
70. Thompson S.N., Borchardt D.B., Wang L.W. Dietary nutrient levels regulate protein and carbohydrate intake, gluconeogenic/glycolytic flux and blood trehalose level in the insect Manduca sexta L. Journal of Comparative Physiology B 2003, 173:149-163.
71. van der Have T.M., de Jong G. Adult size in ectotherms: temperature effects on growth and differentiation. Journal of Theoretical Biology 1996, 183:329-340.
72. Van Handel E. Fuel metabolism of the mosquito (Culex quinquefasciatus) embryo. Journal of Insect Physiology 1993, 39:831-833.
73. Van Voorhies W.A. Bergmann size clines: a simple explanation for their occurrence in ectotherms. Evolution 1996, 50:1259-1264.
74. Van't Hof A.E., Zwaan B.J., Saccheri I.J., Daly D., Bot A.N.M., Brakefield P.M. Characterization of 28 microsatellite loci for the butterfly Bicyclus anynana. Molecular Ecology Notes 2005, 5:169-172.
75. Westerlund S.A., Hoffmann K.H. Rapid quantification of juvenile hormones and their metabolites in insect haemolymph by liquid chromatography-mass spectrometry (LC-MS). Analytical and Bioanalytical Chemistry 2004, 379:540-543.
76. Windig J.J. Reaction norms and the genetic-basis of phenotypic plasticity in the wing pattern of the butterfly Bicyclus anynana. Journal of Evolutionary Biology 1994, 7:665-695.
77. Winkler D.W., Wallin K. Offspring size and number-a life-history model linking effort per offspring and total effort. American Naturalist 1987, 129:708-720.
78. Yampolski L.Y., Scheiner S.M. Why larger offspring at lower temperatures? A demographic approach. American Naturalist 1996, 147:86-100.
79. Zera A.J. The endocrine regulation of wing polymorphism in insects: state of the art, recent surprises, and future directions. Integrative and Comparative Biology 2003, 43:607-616.
80. Zera A.J. Endocrine analysis in evolutionary-developmental studies of insect polymorphism: hormone manipulation versus direct measurement of hormonal regulators. Evolution and Development 2007, 9:499-513.
81. Zera A.J., Harshman L.G., Williams T.D. Evolutionary endocrinology: the developing synthesis between endocrinology and evolutionary genetics. Annual Review of Ecology, Evolution and Systematics 2007, 38:793-817.
82. Zhao Z., Zera A.J. The hemolymph JH titer exhibits a large-amplitude, morph-dependent, diurnal cycle in the wing-polymorphic cricket, Gryllus firmus. Journal of Insect Physiology 2004, 50:93-102.
83. Ziegler R., Van Antwerpen R. Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 2006, 36:264-272.
84. Zijlstra W.G., Steigenga M.J., Koch P.B., Zwaan B.J., Brakefield P.M. Butterfly selected lines explore the hormonal basis of interactions between life histories and morphology. American Naturalist 2004, 163:E76-E87.