Host-parasite arms races and rapid changes in bird egg appearance

American Naturalist

Volumn 179, Issue 5, 2012, Pages 632-648

  Spottiswoode, Claire N ^a,b   Stevens, Martin ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

Brood parasitism; Coevolution; Egg color; Egg pattern; Frequency dependent selection; Vision

Indexed keywords

ADAPTATION; BIRD; BROOD PARASITISM; COEVOLUTION; COLOR; CORRELATION; DEFENSE BEHAVIOR; ECOLOGICAL MODELING; FREQUENCY ANALYSIS; HOST-PARASITE INTERACTION; PASSERINE; PHENOTYPE; PHENOTYPIC PLASTICITY; POLYMORPHISM; PREDATOR-PREY INTERACTION; SELECTION;

AFRICA;

ANOMALOSPIZA IMBERBIS; AVES; PRINIA; PRINIA SUBFLAVA;

ADAPTATION; ANIMAL; ARTICLE; COLOR; EVOLUTION; FEMALE; FINCH; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETICS; GEOGRAPHY; HOST PARASITE INTERACTION; OOCYTE; PHENOTYPE;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; COLOR; FEMALE; FINCHES; GEOGRAPHY; HOST-PARASITE INTERACTIONS; OVUM; PHENOTYPE; POLYMORPHISM, GENETIC; SELECTION, GENETIC;

EID: 84859707269     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/665031     Document Type: Article

References (74)

1. Allen, J. A. 1988. Frequency dependent selection by predators. Philosophical Transactions of the Royal Society B: Biological Sciences 319:485-503.
2. Allen, J. A., and B. Clarke. 1968. Evidence for apostatic selection by wild passerines. Nature 220:501-502.
3. Apanius, V., D. Penn, P. R. Slev, L. R. Ruff, and W. K. Potts. 1997. The nature of selection on the major histocompatibility complex. Critical Reviews in Immunology 17:179-224.
4. Avilés, J. M. 2008. Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proceedings of the Royal Society B: Biological Sciences 275:2345-2352.
5. Avilés, J. M., B. G. Stokke, A. Moksnes, E. Røskaft, and A. P. Møller. 2007. Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behavioral Ecology and Sociobiology 61: 475-485.
6. Beecher, M. D. 1982. Signature systems and kin recognition. American Zoology 22:477-490.
7. Bond, A. B., and A. C. Kamil. 1998. Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature 395:594-596.
8. Bond, A. B., and A. C. Kamil. 2002. Visual predators select for crypticity and polymorphism in virtual prey. Nature 415:609-613.
9. Bond, A. B., and A. C. Kamil. 2006. Spatial heterogeneity, predator cognition, and the evolution of color polymorphism in virtual prey. Proceedings of the National Academy of Sciences of the USA 103:3214-3219.
10. Brooke, M. d. L., and N. B. Davies. 1988. Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature 335: 630-632.
11. Cassey, P., M. Honza, T. Grim, and M. E. Hauber. 2008. The modeling of avian visual perception predicts behavioural rejection responses to foreign egg colours. Biology Letters 4:515-517.
12. Cassey, P., G. Maurer, C. Duval, J. G. Ewen, and M. E. Hauber. 2010. Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens. Behavioral Ecology and Sociobiology 64:1711-1720.
13. Collias, E. C. 1993. Inheritance of egg-colour polymorphisms in the village weaver (Ploceus cucullatus). Auk 110:683-692.
14. Cuthill, I. C. 2006. Color perception. Pages 3-40 in G. E. Hill and K. J. McGraw, eds. Bird coloration. Vol. 1. Mechanisms and measurement. Harvard University Press, Cambridge, MA.
15. Dale, J., D. B. Lank, and H. K. Reeve. 2001. Signaling individual identity versus quality: a model and case studies with ruffs, queleas, and house finches. American Naturalist 158:75-86.
16. Davies, N. B., and M. D. Brooke. 1989. An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. II. Host egg markings, chick discrimination and general discussion. Journal of Animal Ecology 58:225-236.
17. Dawkins, R., and J. R. Krebs. 1979. Arms races between and within species. Proceedings of the Royal Society B: Biological Sciences 205:489-511.
18. Decaestecker, E., S. Gaba, J. Raeymaekers, R. Stoks, L. Van Kerckhoven, D. Ebert, and L. De Meester. 2007. Host-parasite "Red Queen" dynamics archived in pond sediment. Nature 450:870-873.
19. Dieckmann, U., P. Marrow, and R. Law. 1995. Evolutionary cycling in predator-prey interactions: population dynamics and the Red Queen. Journal of Theoretical Biology 176:91-102.
20. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: a study in coevolution. Evolution 18:586-608.
21. Endler, J. A. 1986. Natural selection in the wild. Princeton University Press, Princeton, NJ.
22. Endler, J. A., and P. W. J. Mielke. 2005. Comparing color patterns as birds see them. Biological Journal of the Linnean Society 86: 405-431.
23. Gaba, S., and D. Ebert. 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends in Ecology & Evolution 24: 226-232.
24. Gandon, S., A. Buckling, E. Decaestecker, and T. Day. 2008. Hostparasite coevolution and patterns of adaptation across time and space. Journal of Evolutionary Biology 21:1861-1866.
25. Gorchein, A., C. K. Lima, and P. Cassey. 2009. Extraction and analysis of colourful eggshell pigments using HPLC andHPLC/electrospray ionization tandem mass spectrometry. Biomedical Chromatography 23:602-606.
26. Hanlon, R. T., C.-C. Chiao, L. M. Mäthger, A. Barbosa, K. C. Buresch, and C. Chubb. 2009. Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philosophical Transactions of the Royal Society B: Biological Sciences 364:429-437.
27. Hart, N. S., J. C. Partridge, A. T. D. Bennett, and I. C. Cuthill. 2000a. Visual pigments, cone oil droplets and ocular media in four species of estrildid finch. Journal of Comparative Physiology A 186:681-694.
28. Hart, N. S., J. C. Partridge, I. C. Cuthill, and A. T. D. Bennett. 2000b. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). Journal of Comparative Physiology A 186:375-387.
29. Kennedy, G. Y., and H. G. Vevers. 1976. A survey of avian eggshell pigments. Comparative Biochemistry and Physiology B 55:117-123.
30. Komdeur, J., M. Oorebeek, T. van Overveld, and I. C. Cuthill. 2005. Mutual ornamentation, age, and reproductive performance in the European starling. Behavioral Ecology 16:805-817.
31. Lahti, D. C. 2005. Evolution of bird eggs in the absence of cuckoo parasitism. Proceedings of the National Academy of Sciences of the USA 102:18057-18062.
32. Lahti, D. C. 2006. Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism. Evolution 60:157-168.
33. Lahti, D. C. 2008. Population differentiation and rapid evolution of egg color in accordance with solar radiation. Auk 125:796-802.
34. Lenormand, T. 2002. Gene flow and the limits to natural selection. Trends in Ecology & Evolution 17:183-189.
35. Lively, C. M., and M. F. Dybdahl. 2000. Parasite adaptation to locally common host genotypes. Nature 405:679-681.
36. Lund, U., and C. Agostinelli. 2007. Circular: circular statistics. R package version 0.3-8.
37. Martin, S. J., H. Helanterä, and F. P. Drijfhout. 2011. Is parasite pressure a driver of chemical cue diversity in ants? Proceedings of the Royal Society B: Biological Sciences 278:496-503.
38. May, R., and A. McLean. 2007. Theoretical ecology: principles and applications. Oxford University Press, Oxford.
39. Moksnes, A., E. Røskaft, A. T. Braa, L. Korsnes, H. L. Lampe, and H. C. Pedersen. 1990. Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64-89.
40. Moreno, J., E. Lobato, and J. Morales. 2011. Eggshell blue-green colouration fades immediately after oviposition: a cautionary note about measuring natural egg colours. Ornis Fennica 88:51-56.
41. Newton, A. 1896. A dictionary of birds. Adam & Charles Black, London.
42. Nuismer, S. L., M. Doebeli, and D. Browning. 2005. The coevolutionary dynamics of antagonistic interactions mediated by quantitative traits with evolving variances. Evolution 59:2073-2082.
43. Ödeen, A., and O. Hastad. 2003. Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Molecular Biology and Evolution 20:855-861.
44. Olendorf, R., F. H. Rodd, D. Punzalan, A. E. Houde, C. Hurt, D. N. Reznick, and K. A. Hughes. 2006. Frequency-dependent survival in natural guppy populations. Nature 441:633-636.
45. Osorio, D., and M. Vorobyev. 2005. Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proceedings of the Royal Society B: Biological Sciences 272: 1745-1752.
46. Pietrewicz, A. T., and A. C. Kamil. 1979. Search image formation in the blue jay (Cyanocitta cristata). Science 204:1332-1333.
47. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
48. Ruxton, G. D. 2006. The unequal variance t-test is an underused alternative to Student's t-test and the Mann-Whitney U test. Behavioral Ecology 17:688-690.
49. Schmid-Hempel, P. 2011. Evolutionary parasitology. Oxford University Press, Oxford.
50. Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. Van der Sluijs, et al. 2008. Speciation through sensory drive in cichlid fish. Nature 455:620-627.
51. Siddiqi, A., T. W. Cronin, E. R. Loew, M. Vorobyev, and K. Summers. 2004. Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. Journal of Experimental Biology 207:2471-2485.
52. Sorenson, M. D., and R. B. Payne. 2001. A single, ancient origin of obligate brood parasitism in African finches: implications for hostparasite coevolution. Evolution 55:2550-2567.
53. Spottiswoode, C. N., and M. Stevens. 2010. Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. Proceedings of the National Academy of Sciences of the USA 107:8672-8676.
54. Spottiswoode, C. N., and M. Stevens. 2011. How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences. Proceedings of the Royal Society B: Biological Sciences 278:3566-3573.
55. Stevens, M., and S. Merilaita, eds. 2011. Animal camouflage: from mechanisms to function. Cambridge University Press, Cambridge.
56. Stevens, M., A. Párraga, I. C. Cuthill, J. C. Partridge, and T. Troscianko. 2007. Using digital photography to study animal coloration. Biological Journal of the Linnean Society 90:211-237.
57. Stoddard, M. C., and R. O. Prum. 2008. Evolution of avian plumage color in a tetrahedral colour space: a phylogenetic analysis of New World buntings. American Naturalist 171:755-776.
58. Stoddard, M. C., and M. Stevens. 2010. Pattern mimicry of host eggs by the common cuckoo, as seen through a bird's eye. Proceedings of the Royal Society B: Biological Sciences 277:1387-1393.
59. Stoddard, M. C., and M. Stevens. 2011. Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:2004-2013.
60. Stoddard, M. C., K. Marshall, and R. M. Kilner. 2011. Imperfectly camouflaged eggs: artefact or adaptation? Avian Biology Research 4:196-213.
61. Stokke, B. G., A. Moksnes, and E. Røskaft. 2002. Obligate brood parasites as selective agents for the evolution of egg appearance in passerine birds. Evolution 56:199-205.
62. Summers, K., S. McKeon, J. Sellars, M. Keusenkothen, J. Morris, D. Gloeckner, C. Pressley, et al. 2003. Parasitic exploitation as an engine of diversity. Biological Review 78:639-675.
63. Swynnerton, C. F. M. 1918. Rejections by birds of eggs unlike their own: with remarks on some of the cuckoo problems. Ibis 6:127-154.
64. Takasu, F. 2003. Co-evolutionary dynamics of egg appearance in avian brood parasitism. Evolutionary Ecology Research 5:345-362.
65. Takasu, F. 2005. A theoretical consideration on co-evolutionary interactions between avian brood parasites and their hosts. Ornithological Science 4:65-67.
66. Thompson, J. N. 1998. Rapid evolution as an ecological process. Trends in Ecology & Evolution 18:329-332.
67. Thompson, J. N. 1999. The evolution of species interactions. Science 284: 2116-2118.
68. van Valen, L. 1973. A new evolutionary law. Evolutionary Theory 1: 1-30.
69. Vernon, C. J. 1964. The breeding of the cuckoo weaver Anomalospiza imberbis in southern Rhodesia. Ostrich 35:260-263.
70. Victoria, J. K. 1972. Clutch characteristics and egg discriminative ability of the African village weaverbird Ploceus cucullatus. Ibis 114: 367-376.
71. Vorobyev, M., and D. Osorio. 1998. Receptor noise as a determinant of colour thresholds. Proceedings of the Royal Society B: Biological Sciences 265:351-358.
72. Woolhouse, M. E. J., J. P. Webster, E. Domingo, B. Charlesworth, and B. R. Levin. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics 32:569-577.
73. Yang, C., W. Liang, Y. Cai, S. Shi, F. Takasu, A. P. Møller, A. Antonov, et al. 2010. Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host. PLoS ONE 5:e10816.
74. Yoder, J. B., and S. L. Nuismer. 2010. When does coevolution promote diversification? American Naturalist 176:802-817.