Age-related changes in thoracic mass: Possible reallocation of resources to reproduction in butterflies

Biological Journal of the Linnean Society

Volumn 86, Issue 3, 2005, Pages 363-380

  Stjernholm, Fredrik ^a   Karlsson, Bengt ^a   Boggs, Carol L ^b  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Comparative study; Degree of polyandry; Flight muscle breakdown; Histolysis; Mating system; Nymphalidae; Pieridae; Reproductive investment

Indexed keywords

BUTTERFLY; MUSCLE; REPRODUCTIVE POTENTIAL; RESOURCE ALLOCATION;

HEXAPODA; INSECTA; NYMPHALIDAE; PAPILIONOIDEA; PIERIDAE; PIERIS NAPI;

EID: 27744543427     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2005.00542.x     Document Type: Article

References (74)

1. Andersen NM. 1973. Seasonal polymorphism and developmental changes in organs of flight and reproduction in bivoltine pondskaters (Hem. gerridae). Entomologica Scandinavica 4: 1-20.
2. Aubert J, Barascud B, Descimon H, Michel F. 1996. Systématique moléculaire des Argynnes (Lepidoptera: Nymphalidae). Comptes Rendus de l'Académie des Sciences. Sciences de la Vie 319: 647-651.
3. Baker HG, Baker I. 1973. Amino acids in nectar and their evolutionary significance. Nature 241: 543-545.
4. Berwaerts K, Van Dyck H, Aerts P. 2002. Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Functional Ecology 16: 484-491.
5. Bissoondath C, Wiklund C. 1995. Protein content of spermatophores in relation to monandry/polyandry in butterflies. Behavioral Ecology and Sociobiology 37: 365-371.
6. Boggs CL. 1981. Nutritional and life-history determinants of resource allocation in holometabolus insects. American Naturalist 117: 692-709.
7. Boggs CL. 1986. Reproductive strategies of female butterflies: variation in and constraints on fecundity. Ecological Entomology 11: 7-15.
8. Brinkhurst RO. 1959. Alary polymorphism in the gerroidea (Hemiptera-Heteroptera). Journal of Animal Ecology 28: 211-230.
9. Burns JM. 1968. Mating frequency in natural populations of skippers and butterflies as determined by spermatophore counts. Proceedings of the National Academy of Sciences, USA 61: 852-859.
10. Chai P, Srygley RB. 1990. Predation and the flight, morphology, and temperature of neotropical rain-forest butterflies. American Naturalist 135: 748-765.
11. Chapman JA. 1956. Flight-muscle changes during adult life in a scolytid beetle. Nature 177: 1183.
12. Dunlap-Pianka H, Boggs CL, Gilbert LE. 1977. Ovarian dynamics in Heliconiine butterflies: programmed senescence versus eternal youth. Science 197: 487-490.
13. Edwards FJ. 1969. Development and histolysis of the indirect flight muscles in Dysdercus intermedius. Journal of Insect Physiology 15: 1591-1599.
14. Ellers J, Boggs CL. 2004. Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies. Biological Journal of the Linnean Society 82: 79-87.
15. Erhardt A, Rusterholz HP. 1998. Do peacock butterflies (Inachis io L.) detect and prefer nectar amino acids and other nitrogenous compounds? Oecologia 117: 536-542.
16. Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist 125: 1-15.
17. Fischer K, O'Brien DM, Boggs CL. 2004. Allocation of larval and adult resources to reproduction in a fruit-feeding butterfly. Functional Ecology 18: 656-663.
18. Garland T Jr, Dickerman AW, Janis CM, Jones JA. 1993. Phylogenetic analysis of covariance by computer simulation. Systematic Biology 42: 265-292.
19. Geiger HJ. 1981. Enzyme electrophoresis studies of the genetic relationship of Pierid butterflies. I. European taxa. Journal of Research on the Lepidoptera 19: 181-195.
20. Gibo DL, McCurdy JA. 1993. Lipid accumulation by migrating monarch butterflies (Danaus plexippus L.). Canadian Journal of Zoology 71: 76-82.
21. Gilbert LE. 1972. Pollen feeding and reproductive biology of Heliconius butterflies. Proceedings of the National Academy of Sciences, USA 69: 1402-1407.
22. Hill CJ. 1989. The effect of adult diet on the biology of butterflies. 2. The common crow butterfly, Euploea core corinna. Oecologia. 81: 258-266.
23. Hill CJ, Pierce NE. 1989. The effect of adult diet on the biology of butterflies. 1. The common imperial blue, Jalmenus evagoras. Oecologia. 81: 249-257.
24. Hocking B. 1952. Autolysis of flight muscles in a mosquito. Nature 69: 1101.
25. Jackson DJ. 1933. Observations on the flight muscles of Sitona weevils. Annals of Applied Biology 20: 731-769.
26. Janet C. 1906. Remplacement des muscles vibrateurs du volume par des colonnes d'adipocytes, ches les fourmis, après le volume nuptial. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences 142: 1095-1097.
27. Janet C. 1907. Histolyse, sans phagocytose, des muscles vibrateurs du volume, ches les reines des fourmis. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences 144: 393-396.
28. Johnson B. 1953. Flight muscle autolysis and reproduction in aphids. Nature 172: 813.
29. Johnson B. 1957. Studies on the degeneration of the flight muscles of alate aphids-I. A comparative study of the occurrence of muscle breakdown in relation to reproduction in several species. Journal of Insect Physiology 1: 248-256.
30. Jones RG, Davies WL, Hung ACF, Vinson SB. 1978. Insemination-induced histolysis of the flight musculature in fire ants (Solenopsis spp.): an ultrastructural study. American Journal of Anatomy 151: 603-610.
31. Kaitala A. 1988. Wing muscle dimorphism: two reproductive pathways of the waterstrider Gerris thoracicus in relation to habitat instability. Oikos. 53: 222-228.
32. Kaitala A, Huldén L. 1990. Significance of spring migration and flexibility in flight-muscle histolysis in waterstriders (Heteroptera, Gerridae). Ecological Entomology 15: 409-418.
33. Karlsson B. 1994. Feeding habits and change of body composition with age in three nymphalid butterfly species. Oikos 69: 224-230.
34. Karlsson B. 1995. Resource allocation and mating systems in butterflies. Evolution 49: 955-961.
35. Karlsson B. 1996. Male reproductive reserves in relation to mating systems in butterflies: a comparative study. Proceedings of the Royal Society of London B 263: 187-192.
36. Karlsson B. 1998. Nuptial gifts, resource budgets and reproductive output in a polyandrous butterfly. Ecology 79: 2931-2940.
37. Kemp DJ. 2002. Butterfly contest and flight physiology: why do old males fight harder? Behavioral Ecology 13: 456-461.
38. Kobayashi M, Ishikawa H. 1993. Breakdown of indirect flight muscles of alate aphids (Acyrthosiphon pisum) in relation to their flight, feeding and reproductive behaviour. Journal of Insect Physiology 39: 549-554.
39. Marden JH. 1995. How insects learned to fly. The Sciences 35 (6): 26-30.
40. Marden JH. 2000. Variability in the size, composition and function of insect flight muscles. Annual Review of Physiology 62: 157-178.
41. Marden JH, Chai P. 1991. Aerial predation and butterfly design: how palatability, mimicry, and the need for evasive flight constrains mass allocation. American Naturalist 138: 15-36.
42. Mattson WJ. 1980. Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11: 119-161.
43. May PG. 1992. Flower selection and the dynamics of lipid reserves in two nectarivorous butterflies. Ecology 73: 2181-2191.
44. 2 on larval food and butterfly nectar amino acid preference in Coenonympha pamphilus L. Behavioral Ecology and Sociobiology 54: 36-43.
45. Moore RA, Singer MC. 1987. Effects of maternal age and adult diet on egg weight in the butterfly Euphydryas editha. Ecological Entomology 12: 401-408.
46. Nair CRM, Prabhu VKK. 1985. Entry of proteins from degenerating flight muscles into oocytes in Dysdercus cingulatus (Heteroptera: Pyrrhocoridae). Journal of Insect Physiology 31: 383-388.
47. Norberg U, Leimar O. 2002. Spatial and temporal variation in flight morphology in the butterfly Melitaea cinxia (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society 77: 445-453.
48. Nylin S, Nyblom K, Ronquist F, Janz N, Belicek J, Källersjö M. 2001. Phylogeny of Polygonia, Nymphalis and related butterflies (Lepidoptera: Nymphalidae): a total-evidence approach. Zoological Journal of the Linnean Society 132: 441-468.
49. O'Brien DM, Boggs CL, Fogel ML. 2003. Pollen feeding in the butterfly Heliconius charitonia: isotopic evidence for essential amino acid transfer from pollen to eggs. Proceedings of the Royal Society of London B 270: 2631-2636.
50. O'Brien DM, Fogel M, Boggs CL. 2002. Renewable and non renewable resources: amino acid turnover and allocation to reproduction in Lepidoptera. Proceedings of the National Academy of Sciences, USA 99: 4413-4418.
51. Pullin AS. 1987. Adult feeding time, lipid accumulation, and overwintering in Aglais urticae and Inachis io (Lepidoptera: Nymphalidae). Journal of Zoology 211: 631-641.
52. Rankin MA, Burchsted JCA. 1992. The cost of migration in insects. Annual Review of Entomology 37: 533-559.
53. Ready NE, Josephson RK. 1982. Flight muscle development in a hemimetabolous insect. Journal of Experimental Zoology 220: 49-56.
54. Roff DA. 1986. The evolution of wing dimorphism in insects. Evolution 40 (5): 1009-1020.
55. Rusterholz HP, Erhardt A. 2000. Can nectar properties explain sex-specific flower preferences in the Adonis blue butterfly Lysandra bellargus? Ecological Entomology 25: 81-90.
56. Sattler K. 1991. A review of wing reduction in Lepidoptera. Bulletin of the British Museum (Natural History), Entomology 60 (2): 243-288.
57. Scott JA. 1974. Mate-locating behaviour of butterflies. American Midland Nataturalist 91: 103-117.
58. Shiga S, Kogawauchi S, Yasuyama K, Yamaguchi T. 1991. Flight behaviour and selective degeneration of flight muscles in the adult cricket (Gryllus bimaculatus). Journal of Experimental Biology 155: 661-667.
59. Solbreck C. 1986. Wing and flight muscle polymorphism in a lygaeid bug, Horvathiolus gibbicollis: determinants and life history consequences. Ecological Entomology 11: 435-444.
60. StatSoft. 1999. STATISTICA for Windows. http://www. statsoft.com
61. Stjernholm F, Karlsson B. 2000. Nuptial gifts and the use of body resources for reproduction in the green-veined white butterfly Pieris napi. Proceedings of the Royal Society of London B 267: 807-811.
62. Svärd L, Wiklund C. 1989. Mass and production rate of ejaculates in relation to monandry/polyandry in butterflies. Behavioral Ecology and Sociobiology 24: 395-402.
63. Tanaka S. 1991. De-alation and its influences on egg production and flight muscle histolysis in a cricket (Velarifictorus parvus) that undergoes inter-reproductive migration. Journal of Insect Physiology 37: 517-523.
64. Tanaka S. 1993. Allocation of resources to egg production and flight muscle development in a wing dimorphic cricket, Modicogryllus confirmatus. Journal of Insect Physiology 39: 493-498.
65. Tanaka S, Suzuki Y. 1998. Physiological trade-offs between reproduction, flight capability and longevity in a wing-dimorphic cricket, Modicogryllus confirmatus. Journal of Insect Physiology 44: 121-129.
66. Telang A, Buck NA, Wheeler DE. 2002. Response of storage protein levels to variation in dietary protein levels. Journal of Insect Physiology 48: 1021-1029.
67. Troyer HL, Burks CS, Lee RE. 1996. Phenology of cold hardiness in reproductive and migrant monarch butterflies (Danaus plexippus) in southwest Ohio. Journal of Insect Physiology 42: 633-642.
68. Wagner DL, Liebherr JK. 1992. Flightlessness in insects. Trends in Ecology and Evolution 7: 216-220.
69. Wahlberg N, Weingartner E, Nylin S. 2003. Towards a better understanding of the higher systematics of Nymphalidae (Lepidoptera: Papilionoidea). Molecular Phylogenetics and Evolution 28: 473-484.
70. Wheeler DE, Tuchinskaya I, Buck NA, Tabashnik BE. 2000. Hexameric storage proteins during metamorphosis and egg production in the diamondback moth, Plutella xylostella (Lepidoptera). Journal of Insect Physiology 46: 951-958.
71. Wickman P-O, Wiklund C. 1983. Territorial defense and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Animal Behavior 31: 1206-1216.
72. Wiklund C, Forsberg J. 1991. Sexual size dimorphism in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and satyridae. Oikos 60: 373-381.
73. Wiklund C, Karlsson B, Leimar O. 2001. Sexual conflict and cooperation in butterfly reproduction: a comparative study of polyandry and female fitness. Proceedings of the Royal Society of London B 269: 1661-1667.
74. Zera AJ, Denno RF. 1997. Physiology and ecology of dispersal polymorphism in insects. Annual Review of Entomology 42: 207-230.