Take-off flight performance in the butterfly Pararge aegeria relative to sex and morphology: A quantitative genetic assessment

Evolution

Volumn 62, Issue 10, 2008, Pages 2525-2533

  Berwaerts, Koen ^a   Matthysen, Erik ^a   Van Dyck, Hans ^b  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Flight morphology; Flight performance; Genetic correlation; Heritability; Pararge aegeria; Speckled wood butterfly; Territorial behavior

Indexed keywords

ACCELERATION; BEHAVIORAL RESPONSE; BODY MASS; BODY TEMPERATURE; BUTTERFLY; EVOLUTIONARY BIOLOGY; FITNESS; FLIGHT ACTIVITY; GENETIC ANALYSIS; GENETIC VARIATION; HERITABILITY; MAXIMUM LIKELIHOOD ANALYSIS; MORPHOLOGY; PERCHING BEHAVIOR; SEX-RELATED DIFFERENCE;

ANIMAL; ARTICLE; BUTTERFLY; FEMALE; FLYING; FORELIMB; GENETIC VARIABILITY; HISTOLOGY; MALE; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

ANIMALS; BUTTERFLIES; FEMALE; FLIGHT, ANIMAL; GENETIC VARIATION; MALE; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; WING;

PAPILIONOIDEA; PARARGE AEGERIA;

EID: 53149136224     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00456.x     Document Type: Article

References (72)

1. Berwaerts, K., and H. Van Dyck. 2004. Take-off performance under optimal and suboptimal thermal conditions in the butterfly Pararge aegeria. Oecologia 141 : 536 545.
2. Berwaerts, K., H. Van Dyck, and P. Aerts. 2002. Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct. Ecol. 16 : 484 491.
3. Berwaerts, K., P. Aerts, and H. Van Dyck. 2006. On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria. Biol. J. Linn. Soc. 89 : 675 687.
4. Biewener, A. A., and R. J. Full. 1990. Force platform and kinematic analysis. Pp. 45 73 in A. A. Biewener, ed. Biomechanics - structures and systems. A practical approach. Oxford Univ. Press, Oxford.
5. Brodie, E. D., III. 1989. Genetic correlations between morphology and antipredator behaviour in natural populations of the garter snake Thamnophis ordinoides. Nature 342 : 542 543.
6. Brodie, E. D. 1993. Homogeneity of the genetic variance-covariance matrix for antipredator traits in two natural populations of the garter snake Thamnophis ordinoides. Evolution 47 : 844 854.
7. Caldwell, R. L., and J. P. Hegmann. 1969. Heritability of flight duration in the milkweed bug Lygaeus kalmii. Nature 223 : 91 92.
8. Colvin, J., and A. G. Gatehouse. 1993. The reproduction-flight syndrome and the inheritance of tethered-flight activity in the cotton-bollworm moth, Heliothis armigera. Physiol. Entomol. 18 : 16 22.
9. Cowley, D. E., and W. R. Atchley. 1988. Quantitative genetics of Drosophila melanogaster. II. heritabilities and genetic correlations between sexes for head and thorax traits. Genetics 119 : 421 433.
10. Crompton, B., J. Thomason, and A. J. McLachlan. 2003. Mating in a viscous universe: the race is to the agile, not to the swift. Proc. R. Soc. Lond. B 270 : 1991 1995.
11. Dudley, R. 2000. Biomechanics of insect flight: form, function, evolution. Princeton Univ. Press, Princeton, NJ.
12. 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.
13. Ellers, J., and C. L. Boggs. 2003. The evolution of wing color: male mate choice opposes adaptive wing color divergence in Colias butterflies. Evolution 57 : 1100 1106.
14. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Longman, Essex.
15. Forsman, A. 1999. Temperature influence on escape behaviour in two species of pygmy grasshoppers. Ecoscience 6 : 35 40.
16. Groeneveld, E. 1995. REML VCE: a multivariate multi model restricted maximum likelihood (co)variance component estimation package. Ver. 3.2 user's guide. Institute for Animal Husbandry and Animal Behaviour, Federal Research Centre of Agriculture, Mariensee.
17. Gu, H., and W. Danthanarayana. 1992a. Quantitative genetic analysis of dispersal in Epiphyas postvittana. I. Genetic variation in flight capacity. Heredity 68 : 53 60.
18. Gu, H., and W. Danthanarayana. 1992b. Quantitative genetic analysis of dispersal in Epiphyas postvittana. II. Genetic covariations between flight capacity and life-history traits. Heredity 68 : 61 69.
19. Gu, H., and J. S. F. Barker. 1995. Genetic and phenotypic variation in flight ability in the cactophilic Drosophila species, D. aldrichi and D. buzzatii. Entomol. Exper. Appl. 76 : 25 35.
20. Gullan, P. J., and P. S. Cranston. 2005. The insects. an outline of entomology 3rd ed. Blackwell Publishing, Oxford.
21. Haag, C. R., M. Saastamoinen, J. H. Marden, and I. Hanski. 2005. A candidate locus for variation in dispersal rate in a butterfly metapopulation. Proc. R. Soc. Lond. B 272 : 2449 2456.
22. Henderson, C. R. 1972. Sire evaluation and genetic trends. Pp. 10 41. in Proceedings of the Animal Breeding and Genetics Symposium in honour of Dr. Jay L. Lush. American Society of Animal Science and Dairy Science Association, Champaign, IL.
23. Hill, J. K., C. D. Thomas, and D. S. Blakeley. 1999. Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia 121 : 165 170.
24. Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130 : 195 204.
25. Huey, R. B., and J. G. Kingsolver. 1989. Evolution of thermal sensitivity of ectotherm performance. Trends Ecol. Evol. 4 : 131 135.
26. Hughes, C. L., J. K. Hill, and C. Dytham. 2003. Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. Proc. R. Soc. Lond. B 270 (Suppl. 2 S147 S150.
27. Imafuku, M., and T. Ohtani. 2006. Analysis of coordinated circling and linear flights of a lycaenid butterfly species. Naturwissenschaften 93 : 131 135.
28. Iyengar, V. K., and T. Eisner. 1999. Heritability of body mass, a sexually selected trait, in an arctiid moth (Utetheisa ornatrix). Proc. Natl. Acad. Sci. USA 96 : 9169 9171.
29. Jensen, H., B.-E. Sæther, T. H. Ringsby, J. Tufto, S. C. Griffith, and H. Ellegren. 2003. Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus). J. Evol. Biol. 16 : 1296 1307.
30. Karlsson, B. 1994. Feeding-habits and change of body-composition with age in 3 nymphalid butterfly species. Oikos 69 : 224 230.
31. Karlsson, B. 1995. Resource allocation and mating systems in butterflies. Evolution 49 : 955 961.
32. Karlsson, B., and H. Van Dyck. 2005. Does habitat fragmentation affect temperature-related life-history traits? A laboratory test with a woodland butterfly. Proc. R. Soc. Lond. B 272 : 1257 1263.
33. Karlsson, B., and P.-O. Wickman. 1990. Increase in reproductive effort as explained by body size and resource allocation in the speckled wood butterfly, Pararge aegeria (L.). Funct. Ecol. 4 : 609 617.
34. Karlsson, B., and C. Wiklund. 2005. Butterfly life history and temperature adaptations:dry open habitats select for increased fecundity and longevity. J. Anim. Ecol. 74 : 99 104.
35. Keil S., H. Gu, and S. Dorn. 2001. Diel patterns of locomotor activity in Cydia pomonella: age and sex related differences and effects of insect hormone mimics. Ecol. Entomol. 26 : 306 314.
36. Kemp, D. J. 2002. Butterfly contests and flight physiology: why do older males fight harder? Behav. Ecol. 13 : 456 461.
37. Kemp, D. J., C. Wiklund, and H. Van Dyck. 2006. Contest behavior in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance. Behav. Ecol. Sociobiol. 59 : 403 411.
38. Kingsolver, J. G. and R. J. Moffat 1982. Thermoregulation and the determinants of heat transfer in Colias butterflies. Oecologia 53 : 27 33.
39. Knott, S. A., R. M. Sibly, R. H. Smith, and H. Möller. 1995. Maximum likelihood estimation of genetic parameters in life-history studies using the 'Animal Model'. Funct. Ecol. 9 : 122 126.
40. Kronfrost, M. R., L. G. Young, D. D. Kapan, C. McNeely, R. J. O'Neill, and L. E. Gilbert. 2006. Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proc. Natl. Acad. Sci. USA 103 : 6575 6580.
41. Lee, S. J., M. S. Witter, I. C. Cuthill, and A. R. Goldsmith. 1996. Reduction in escape performance as a cost of reproduction in gravid starlings, Sturnus vulgaris. Proc. R. Soc. Lond. B 263 : 619 624.
42. Lessells, C. M., and P. T. Boag. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104 : 116 121.
43. Lynch, M., and B. Walsh. 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Inc., Sunderland, MA.
44. Marden, J. H., M. R. Wolf, and K. E. Weber. 1997. Aerial performance of Drosophila melanogaster from populations selected for upwind flight ability. J. Exp. Biol. 200 : 2747 2755.
45. Merckx, T., B. Karlsson, and H. Van Dyck. 2006. Sex- and landscape-related differences in flight ability under suboptimal temperatures in a woodland butterfly. Funct. Ecol. 20 : 436 441.
46. Nudds, R. L., and D. M. Bryant. 2000. The energetic cost of short flights in birds. J. Exp. Biol. 203 : 1561 1572.
47. Nylin, S., P.-O. Wickman, and C. Wiklund. 1995. Life cycle regulation and life history plasticity in the speckled wood butterfly: are reaction norms predictable? Biol. J. Linn. Soc. 55 : 143 157.
48. Optimas. 1999. Optimas 6.51. User's guide and technical reference. Optimas Corporation, Bothell, Washington.
49. Pearse, F. K., and N. D. Murray. 1982. Sex and variability in the common brown butterfly Heteronympha merope merope (Lepidoptera: Satyrinae). Evolution 36 : 1251 1264.
50. Rutowski, R. L. 1997. Sexual dimorphism, mating systems and ecology in butterflies. Pp. 257 272 in J. C. Choe and B. J. Crespi, eds. The evolution of mating systems in insects and Arachnids. Cambridge Univ. Press, Cambridge.
51. Scott, J. A. 1974. Mate-locating behavior in butterflies. Am. Midl. Nat. 91 : 103 117.
52. Shreeve, T. G. 1984. Habitat selection, mate location, and micro-climatic constraints on the activity of the speckled wood butterfly Pararge aegeria. Oikos 42 : 371 377.
53. Shreeve, T. G. 1986. Egg-laying by the speckled wood butterfly (Pararge aegeria): the role of female behaviour, host plant abundance and temperature. Ecol. Entomol. 11 : 229 236.
54. Shreeve, T. G. 1987. The mate location behaviour of the male speckled wood butterfly, Pararge aegeria, and the effect of phenotypic differences in hind-wing spotting. Anim. Behav. 35 : 682 690.
55. Shreeve, T. G. 1990. The movements of butterflies. Pp. 512 532 in O. Kudrna, ed. Butterflies of Europe: introduction to lepidopterology, Aula-Verlag Wiesbaden, Germany.
56. Shuster, S. M., and M. J. Wade 2003. Mating systems and strategies. Monographs in behavior and ecology. Princeton Univ. Press, Princeton, NJ.
57. Srygley, R. B. and Dudley, R. 1993. Correlations of the position of center of body mass with butterfly escape tactics. J. Exp. Biol. 174 : 155 166.
58. Stirling, G., D. Roff, and D. Fairbairn. 1999. Four characters in a trade-off: dissecting their phenotypic and genetic relations. Oecologia 120 : 492 498.
59. Van Dyck, H. 2003. Mate location, a matter of design? Adaptive morphological variation in the speckled wood butterfly. Pp. 353 366 in W. B. Watt, C. L. Boggs and P. R. Ehrlich, eds. Butterflies: ecology and evolution taking flight. Univ. of Chicago Press, Chicago.
60. Van Dyck, H., and E. Matthysen. 1998. Thermoregulatory differences between phenotypes in the speckled wood butterfly (Pararge aegeria L.): hot perchers and cold patrollers. Oecologia 114 : 326 334.
61. Van Dyck, H., and E. Matthysen. 1999. Habitat fragmentation and insect flight: a changing 'design' in a changing landscape? Trends Ecol. Evol. 14 : 172 174.
62. 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.
63. 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 L.). Ecol. Entomol. 23 : 465 472.
64. Watt, W. B., C. B. Wheat, E. H. Meyer, and J.-F. Martin. 2003. Adaptation at specific loci. VII. Natural selection, dispersal and the diversity of molecular-functional variation patterns among butterfly species complexes (Colias: Lepidoptera, Pieridae). Mol. Ecol. 12 : 1265 1275.
65. Weber, K. E. 1996. Large genetic change at small fitness cost in large populations of Drosophila melanogaster selected for wind tunnel flight: rethinking fitness surfaces. Genetics 144 : 205 213.
66. Wickman, P. O. 1992. Sexual selection and butterfly design - a comparative study. Evolution 46 : 1525 1536.
67. Wickman, P.-O., and B. Karlsson. 1989. Abdomen size, body size and the reproductive effort of insects. Oikos 56 : 209 214.
68. 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.
69. Wiklund, C., and A. Persson. 1983. Fecundity, and the relation of egg weight variation to offspring fitness in the speckled wood butterfly Pararge aegeria, or why don't butterfly females lay more eggs? Oikos 40 : 53 63.
70. 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.
71. Winter, D. A. 1990. Biomechanics and motor control of human movement. John Wiley and Sons, Waterloo.
72. Zera, A. J., and R. F. Denno. 1997. Physiology and ecology of dispersal polymorphism in insects. Annu. Rev. Entomol. 42 : 207 231.