Sensory limitations and the maintenance of colour polymorphisms: Viewing the 'alba' female polymorphism through the visual system of male Colias butterflies

Functional Ecology

Volumn 28, Issue 5, 2014, Pages 1197-1207

  Limeri, Lisa B ^a   Morehouse, Nathan I ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Colias eurytheme; Colias philodice; Colour vision; Mate choice; Mate discrimination; Receptor noise limited visual model

Indexed keywords

COLIAS; COLIAS EURYTHEME; COLIAS PHILODICE; PAPILIONOIDEA;

EID: 84908283416     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12244     Document Type: Article

References (48)

1. Ae, S.A. (1959) A study of hybrids in Colias (Lepidoptera, Pieridae). Evolution, 13, 64-88.
2. Awata, H., Wakakuwa, M. & Arikawa, K. (2009) Evolution of color vision in pierid butterflies: blue opsin duplication, ommatidial heterogeneity and eye regionalization in Colias erate. Journal of Comparative Physiology A, 195, 401-408.
3. Briscoe, A.D. (2008) Reconstructing the ancestral butterfly eye: focus on the opsins. Journal of Experimental Biology, 211, 1805-1813.
4. Chamberlain, N.L., Hill, R.I., Kapan, D.D., Gilbert, L.E. & Kronforst, M.R. (2009) Polymorphic butterfly reveals the missing link in ecological speciation. Science, 326, 847-850.
5. Chittka, L., Skorupski, P. & Raine, N.E. (2009) Speed-accuracy tradeoffs in animal decision making. Trends in Ecology and Evolution, 24, 400-407.
6. Chunco, A.J., McKinnon, J.S. & Servedio, M.R. (2007) Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution, 61, 2504-2515.
7. Cook, S.E., Vernon, J.G., Bateson, M. & Guilford, T. (1994) Mate choice in the polymorphic butterfly, Papilio dardanus: male-like females may avoid sexual harassment. Animal Behaviour, 47, 389-397.
8. Cooke, F. & McNally, C.M. (1975) Mate selection and color preferences in Lesser Snow Geese. Behaviour, 53, 151-170.
9. Endler, J.A. & Mielke, P.W. (2005) Comparing entire colour patterns as birds see them. Biological Journal of the Linnean Society, 86, 405-431.
10. Forsman, A., Anhesjo, J., Caesar, S. & Karlsson, M. (2008) A model of ecological and evolutionary consequences of color polymorphism. Ecology, 89, 34-40.
11. Gilchrist, G.W. & Rutowski, R.L. (1986) Adaptive and incidental consequences of the alba polymorphism in an agricultural population of Colias butterflies: female size, fecundity, and differential dispersion. Oecologia, 68, 235-240.
12. Giurfa, M. & Vorobyev, M. (1998) The angular range of achromatic target detection by honey bees. Journal of Comparative Physiology A, 183, 101-110.
13. Giurfa, M., Vorobyev, M., Brandt, R., Posner, B. & Menzel, R. (1997) Discrimination of coloured stimuli by honeybees: alternative use of achromatic and chromatic signals. Journal of Comparative Physiology A, 180, 235-243.
14. Graham, S.M., Watt, W.B. & Gall, L.F. (1980) Metabolic resource allocation vs. mating attractiveness: adaptive pressures on the "alba" polymorphism of Colias butterflies. Proceedings of the National Academy of Science, 77, 3615-3619.
15. Grula, J.W. & Taylor, O.R. (1980) The effect of X-chromosome inheritance on mate-selection behavior in the sulfur butterflies, Colias eurytheme and C. philodice. Evolution, 34, 688-695.
16. Hempel de Ibarra, N., Giurfa, M. & Vorobyev, M. (2002) Discrimination of coloured patterns by honeybees through chromatic and achromatic cues. Journal of Comparative Physiology A, 188, 503-512.
17. Kelber, A. (2006) Invertebrate colour vision. Invertebrate Vision (eds E.J. Warrant & D.E. Nilsson ), pp. 250-290. Cambridge University Press, Cambridge, UK.
18. Kelber, A. & Osorio, D. (2010) From spectral information to animal colour vision: experiments and concepts. Proceedings of the Royal Society of London B Biological Sciences, 277, 1617-1625.
19. Kelber, A., Vorobyev, M. & Osorio, D. (2003) Animal colour vision: behavioural tests and physiological concepts. Biological Reviews of the Cambridge Philosophical Society, 78, 81-118.
20. Kemp, D. (2006) Heightened phenotypic variation and age-based fading of ultraviolet butterfly wing coloration. Evolutionary Ecology Research, 8, 515-527.
21. Kemp, D.J. & Macedonia, J.M. (2007) Male mating bias and its potential reproductive consequence in the butterfly Colias eurytheme. Behavioral Ecology and Sociobiology, 61, 415-422.
22. Koshitaka, H., Arikawa, K. & Kinoshito, M. (2011) Intensity contrast as a crucial cue for butterfly landing. Journal of Comparative Physiology A, 197, 1105-1112.
23. Koshitaka, H., Kinoshita, M., Vorobyev, M. & Arikawa, K. (2008) Tetrachromacy in a butterfly that has eight varieties of spectral receptors. Proceedings of the Royal Society: Biological Sciences, 275, 947-954.
24. Kronforst, M.R., Young, L.G., Kapan, D.D., McNeely, C., O'Neill, R.J. & Gilbert, L.E. (2006) Linkage of butterfly mate preference and wing color preference cue at the genomic location of wingless. Proceedings of the National Academy of Sciences of the United States of America, 103, 6575-6580.
25. Land, M.F. & Nilsson, D.E. (2012) Animal Eyes, 2nd edn. Oxford University Press, New York, New York, USA.
26. Limeri, L. & Morehouse, N.I. (2014) Data from: Sensory limitations and the maintenance of color polymorphisms: viewing the 'alba' female polymorphism through the visual system of male Colias butterflies. Dryad Digital Repository. doi:10.5061/dryad.nd358.
27. Lorkovic, Z. & Herman, C. (1961) The solution of a long outstanding problem in the genetics of dimorphism in Colias. Journal of the Lepidopterists' Society, 15, 43-55.
28. McKinnon, J.S. & Pierotti, M.R. (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Molecular Ecology, 19, 5101-5125.
29. Morehouse, N.I. & Rutowski, R.L. (2010) In the eyes of the beholders: female mate choice and avian predation risk associated with an exaggerated male butterfly color. American Naturalist, 176, 768-784.
30. Nakanishi, Y., Watanabe, M. & Ito, T. (2000) Differences in lifetime reproductive output and mating frequency of two female morphs of sulfur butterfly, Colias erate (Lepidoptera: Pieridae). Journal of Research on the Lepidoptera, 35, 1-8.
31. Nielsen, M.G. & Watt, W.B. (2000) Interference competition and sexual selection promote polymorphism in Colias (Lepidoptera, Pieridae). Functional Ecology, 14, 718-730.
32. Nijhout, H.F. (2003) Polymorphic mimicry in Papilio dardanus: mosaic dominance, big effects, and origins. Evolution & Development, 5, 579-592.
33. Ogawa, Y., Awata, H., Wakakuwa, M., Kinoshita, M., Stavenga, D.G. & Arikawa, K. (2012) Coexpression of three middle wavelength-absorbing visual pigments in sexually dimorphic photoreceptors of the butterfly Colias erate. Journal of Comparative Physiology A, 198, 857-867.
34. Ogawa, Y., Kinoshita, M., Stavenga, D.G. & Arikawa, K. (2013) Sex-specific retinal pigmentation results in sexually dimorphic long-wavelength-sensitive photoreceptors in the Eastern Pale Clouded Yellow butterfly, Colias erate. Journal of Experimental Biology, 216, 1916-1923.
35. Pirih, P., Arikawa, K. & Stavenga, D. (2010) An expanded set of photoreceptors in the Eastern Pale Clouded Yellow butterfly, Colias erate. Journal of Comparative Physiology A, 196, 501-517.
36. Robertson, H.M. (1985) Female dimorphism and mating behaviour in a damselfly, Ischnura ramburi: females mimicking males. Animal Behaviour, 33, 805-809.
37. Rutowski, R.L., Macedonia, J.M., Merry, J.W., Morehouse, N.I., Yturralde, K., Taylor-Taft, L. et al. (2007) Iridescent ultraviolet signal in the orange sulphur butterfly (Colias eurytheme): spatial, temporal and spectral properties. Biological Journal of the Linnean Society, 90, 349-364.
38. Scott, J.A. (1986) The Butterflies of North America: A Natural History and Field Guide. Stanford University Press, Stanford.
39. Sherratt, T.N. (2008) The evolution of female-limited polymorphisms in damselflies: a signal detection model. Ecology Letters, 4, 22-29.
40. Siddiqi, A., Cronin, T.W., Loew, E.R., Vorobyev, M. & Summers, K. (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. The Journal of Experimental Biology, 207, 2471-2485.
41. Silberglied, R.E. & Taylor, O.R. (1978) Ultraviolet reflectance and its behavioral role in courtship of sulfur butterflies Colias eurytheme and C. philodice (Lepidoptera, Pieridae). Behavioral Ecology and Sociobiology, 3, 203-243.
42. Sirot, L.K., Brockmann, H.J., Marnis, C. & Muschett, G. (2003) Maintenance of a female-limited polymorphism in Ischnura ramburi (Zygoptera: Coenagrionidae). Animal Behaviour, 66, 763-775.
43. Van Gossum, H.V., Stoks, R. & De Bruyn, L. (2001) Frequency-dependent male mate harassment and intra-specific variation in its avoidance by females of the damselfly Ischnura elegans. Behavioral Ecology and Sociobiology, 51, 69-75.
44. Vorobyev, M. & Osorio, D. (1998) Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society B: Biological Sciences, 265, 351-358.
45. Vorobyev, M., Brandt, R., Peitsch, D., Laughlin, S.B. & Menzel, R. (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vision Research, 41, 639-653.
46. Watt, W.B. (1995) Decent with modification: evolutionary study of Colias in the tradition of Charles Remington. Journal of Lepidopterists' Society, 49, 272-284.
47. Wickelgren, W.A. (1977) Speed-accuracy tradeoff and information processing dynamics. Acta Psychologica, 41, 67-85.
48. Wittkopp, P.J., Stewart, E.E., Arnold, L.L., Neidert, A.H., Haerum, B.K., Thompson, E.M. et al. (2009) Intraspecific polymorphism to interspecific divergence. Science, 326, 540-544.