The cost of melanization: Butterfly wing coloration under environmental stress

Evolution

Volumn 58, Issue 2, 2004, Pages 360-366

  Talloen, W ^a   Van Dyck, H ^a   Lens, L ^b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Developmental constraint; Fluctuating asymmetry; Resource allocation; Thermoregulation

Indexed keywords

ADAPTATION; BUTTERFLY; COLOR; ENVIRONMENTAL STRESS; FLUCTUATING ASYMMETRY; MELANISM;

ANIMALIA; LEPIDOPTERA; NYMPHALIDAE; PAPILIONOIDEA; PARARGE AEGERIA; POACEAE;

EID: 1642271519     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01651.x     Document Type: Article

References (66)

1. Andersson, M. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ.
2. Arnold, S. J. 1992. Constraints on phenotypic evolution. Am. Nat. 140(Suppl.):S85-S107.
3. Barnes, A., and M. T. Siva-Jothy. 2000. Density-dependent prophylaxis in the mealworm beetle Tenebrio molitor L. (Coleoptera: Tenebrionidae): cuticular melanisation is an indicator of investment in immunity. Proc. R. Soc. Lond. B 267:177-182.
4. Berwaerts, K., H. Van Dyck, E. Vints, and E. Matthysen. 2001. Effect of manipulated wing characteristics and basking posture on thermal properties of the butterfly Pararge aegeria (L.). J. Zool. 255:261-267.
5. Bjorksten, T. A., K. Fowler, and A. Pomiankowski. 2000. What does sexual trait FA tell us about stress? Trends Ecol. Evol. 15: 163-166.
6. Brakefield, P. M. 1987. Industrial melanism: do we have the answers? Trends Ecol. Evol. 2:117-122.
7. Brakefield, P. M., and T. G. Shreeve. 1992. Case studies in evolution. Pp. 197-216 in R. L. H. Dennis, ed. The ecology of butterflies in Britain. Oxford Univ. Press, Oxford, U.K.
8. Clench, H. K. 1966. Behavioral thermoregulation in butterflies. Ecology 47:1021-1034.
9. Cook, L. M., and T. M. G. M. Jacobs. 1983. Frequency and selection on the industrial melanic moth Odontoptera bidentata. Heredity 51:487-494.
10. Dennis, R. L. H., and T. G. Shreeve. 1989. Butterfly morphology variation in the British Isles: the influence of climate, behavioural posture and the hostplant-habitat. Biol. J. Linn. Soc. 38:323-348.
11. Douglas, M. M., and J. W. Grula. 1978. Thermoregulatory adaptations allowing ecological range expansion by the pierid butterfly, Nathalis iole Boisduval. Evolution 32:776-783.
12. Dreisig, H. 1995. Thermoregulation and flight activity in territorial male graylings, Hipparchia semele (Satyridae), and large skippers, Ochlodes venata (Hesperiidae). Oecologia 101:169-176.
13. Ellers, J., and C. L. Boggs. 2002. The evolution of wing color in Colias butterflies: heritability, sex linkage, and population divergence. Evolution 56:836-840.
14. Gilchrist, A. S., R. B. R. Azevedo, L. Partridge, and P. O'Higgins. 2000. Adaptation and constraint in the evolution of Drosophila melanogaster wing shape. Evol. Dev. 2(2):114-124.
15. Graham, S. M., W. B. Watt, and L. F. Gall. 1980. Metabolic resource allocation vs. mating attractions: adaptive pressure on the "alba" polymorphism of Colias butterflies. Proc. Natl. Acad. Sci. USA 77:3615-3619.
16. Guppy, C. S. 1986. The adaptive significance of alpine melanism in the butterfly Parnassius phoebus F. (Lepidoptera: Papilionidae). Oecologia 70:205-213.
17. Hazel, W. N. 1995. The causes and evolution of phenotypic plasticity in pupal color in swallowtail butterflies. Pp. 205-210 in J. M. Scriber, Y. Tsubaki and R. C. Lederhouse, eds. Swallowtail butterflies: the ecology and evolutionary biology. Scientific Publishers, Gainesville, TN.
18. Heinrich, B. 1985. Thermoregulation and flight activity of a satyrine, Coenonympha inornata (Lepidoptera: Satyridae). Ecology 67:593-597.
19. Hill, H. Z. 1992. The function of melanin or six blind people examine an elephant. BioEssays 14:49-56.
20. Hooper, R. E., Y. Tsubaki, and M. T. Siva-Jothy. 1999. Expression of a costly, secondary sexual trait is correlated with age and condition in a damselfly with two male morphs. Physiol. Entomol. 24:364-369.
21. Kearns, P. W. E., I. P. M. Tomlinson, C. J. Veltman, and P. O'Donald. 1992. Non-random mating in Adalia bipunctata (the two-spot ladybird). II. Further tests for female mating preference. Heredity 68:385-389.
22. Kettlewell, H. B. D. 1973. The evolution of melanism: the study of a recurring necessity. Clarendon Press, Oxford, U.K.
23. Kingsolver, J. G., and W. B. Watt. 1983. Thermoregulatory strategies in Colias butterflies: thermal stress and the limits to adaptation in temporally varying environment. Am. Nat. 121:32-55.
24. _. 1984. Mechanistic constraints and optimality models: thermoregulatory strategies in Colias butterflies. Ecology 65:1835-1839.
25. Kooi, R. E., P. M. Brakefield, and W. E. M.-Th. Rossie. 1996. Effects of food plant on phenotypic plasticity in the tropical butterfly Bicyclus anynana. Entomol. Exp. Appl. 80:149-151.
26. Lens, L., S. Van Dongen, S. Kark, and E. Matthysen. 2002. Fluctuating asymmetry as an indicator of fitness: Can we bridge the gap between studies? Biol. Rev. 77:27-38.
27. Littell, R. C., G. A. Milliken, W. W. Stroup, and R. D. Wolfinger. 1996. SAS system for mixed models. SAS Institute Inc., Cary, NC.
28. Majerus, M. E. N. 1998. Melanism: evolution in action. Oxford Univ. Press, Oxford, U.K.
29. Mattson, W. J., Jr. 1980. Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11:119-161.
30. Neter, J., M. H. Kutner, C. J. Nachtsheim, and W. Wasserman. 1996. Applied linear statistical models. 3rd. ed. Irwin, Boston.
31. Nijhout, H. F. 1991. The development and evolution of butterfly wing patterns. Smithsonian Institution Press, Washington, DC.
32. Nylin, S., and K. Gotthard. 1998. Plasticity in life-history traits. Annu. Rev. Entomol. 43:63-83.
33. Nylin, S., P.-O. Wickman, and C. Wiklund. 1989. Seasonal plasticity in growth and development of the speckled wood butterfly, Pararge aegeria (Satyrinae). Biol. J. Linn. Soc. 38:155-171.
34. _. 1995. Life-cycle regulation and life history plasticity in the speckled wood butterfly: Are reaction norms predictable? Biol. J. Linn. Soc. 55:143-157.
35. Ortonne, J.-P. 2002. Photoprotective properties of skin melanin. Brit. J. Dermatol. 146(Suppl. 61):7-10.
36. Palmer, R. A. 1996. Waltzing with asymmetry. Bioscience 46:518-532.
37. Polak, M. 2003. Developmental instability, causes and consequences. Oxford Univ. Press, New York.
38. Pollard, E. 1988. Temperature, rainfall and butterfly numbers. J. Appl. Ecol. 25:819-828.
39. Riley, P. A. 1997. Melanin. Int. J. Biochem. Cell B 29(11):1235-1239.
40. Roland, J. 1982. Melanism and diel activity of alpine Colias (Lepidoptera: Pieridae). Oecologia 53:214-221.
41. Rose, M. R., and G. V. Lauder. 1996. Adaptation. Academic Press, San Diego, CA.
42. Safranek, L., and L. M. Riddiford. 1975. The biology of the black larval mutant of the tobacco hornworm, Manduca sexta. J. Insect Physiol. 21:1931-1938.
43. SAS Institute. 1990. SAS/STAT user's guide. Ver. 6. 4th ed. SAS Institute, Cary, NC.
44. Schmitz, H. 1994. Thermal characterization of butterfly wings. 1. Absorption in relation to different color, surface structure and basking type. J. Therm. Biol. 19:403-412.
45. Senar, J. C. 1999. Plumage coloration as a signal of social status. Pp. 1669-1686 in N. Adams, and R. Slotow, eds. Proceedings of the International Ornithology Congress. Vol. 22.
46. Shreeve, T. G. 1984. Habitat selection, mate-location, and microclimatic constraints on the activity of the speckled wood butterfly Pararge aegeria. Oikos 42:371-377.
47. _. 1986. Egg-laying by the speckled wood (Pararge aegeria): the role of female behaviour, host plant abundance and temperature. Ecol. Entomol. 11:229-236.
48. _. 1992. Adult behaviour. Pp. 22-45 in R. L. H. Dennis, ed. The ecology of butterflies in Britain. Oxford Univ. Press, Oxford, U.K.
49. Stutt, A. D., and P. Willmer. 1998. Territorial defence in speckled wood butterflies: Do the hottest males always win? Anim. Behav. 55:1341-1347.
50. Tolman, T., and R. Lewington. 1997. Butterflies of Britain and Europe. HarperCollins, London.
51. Van Dyck, H. 2003. Mate-location, a matter of design? Adaptive morphological variation in the speckled wood butterfly. Pp. 353-366 in C. L. Boggs, W. B. Watt, and P. R. Ehrlich, eds. Butterflies: ecology and evolution taking flight. Univ. of Chicago Press, Chicago, IL.
52. Van Dyck, H., and E. Matthysen. 1998. Thermoregulatory differences between phenotypes in the speckled wood butterfly: Hot perchers and cold patrollers? Oecologia 114:326-334.
53. Van Dyck, H., and C. Wiklund. 2002. Seasonal butterfly design: morphological plasticity among three developmental pathways relative to sex, flight and thermoregulation. J. Evol. Biol. 15:216-225.
54. Van Dyck, H., E. Matthysen, and A. A. Dhondt. 1997. The effect of wing colour on male behavioural strategies in the speckled wood butterfly. Anim. Behav. 53:39-51.
55. Van Dyck, H., E. Matthysen, and C. Wiklund. 1998. Phenotypic variation in adult morphology and pupal colour within and among families of the speckled wood butterfly Pararge aegeria. Ecol. Entomol. 23:465-472.
56. Verhoog, M. D., C. J. Breuker, and P. M. Brakefield. 1998. The influence of genes for melanism on the activity of the flour moth, Ephestia kuehniella. Anim. Behav. 56:683-688.
57. Wainwright, P. C., and S. M. Reilly. 1994. Ecological morphology: integrative organsimal biology. Univ. of Chicago Press, Chicago, IL.
58. Wasserthal, L. T. 1975. The role of butterfly wings in regulation of body temperature. J. Insect Physiol. 21:1921-1930.
59. Watt, W. B. 1968. Adaptive significance of pigment polymorphisms in Colias butterflies. I. Variation of melanin pigment in relation to thermoregulation. Evolution 22:437-458.
60. Wiernasz, D. 1989. Female choice and sexual selection on male wing melanin pattern in Pieris occidentalis (Lepidoptera). Evolution 43:1672-1682.
61. Wickman, P.-O., and C. Wiklund. 1983. Territorial defence and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim. Behav. 31:1206-1216.
62. Wiklund, C., A. Persson, and P.-O. Wickman. 1983. Larval aestivation and direct development as alternative strategies in the speckled wood butterfly, Pararge aegeria, in Sweden. Ecol. Entomol. 8:233-238.
63. Wilson, K., C. C. Sheena, A. F. Reeson, and J. K. Pell. 2001. Melanin and disease resistance in insects. Ecol. Lett. 4:637-649.
64. Windig, J. J. 1999. Trade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)? Heredity 82:57-68.
65. Windig, J. J., and S. Nylin. 1999. Adaptive wing asymmetry in males of the speckled wood butterfly (Pararge aegeria)? Proc. R. Soc. Lond. B 266:1413-1418.
66. _. 2002. Genetics of fluctuating asymmetry in pupal traits of the speckled wood butterfly (Pararge aegeria). Heredity 89:225-234.