Ectoparasitism in mothers causes higher positional fluctuating asymmetry in their sons: Implications for sexual selection

American Naturalist

Volumn 149, Issue 5, 1997, Pages 955-974

  Polar, Michal ^a,b,c  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c SYRACUSE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUCTUATING ASYMMETRY; HOST-PARASITE INTERACTION; MALE OFFSPRING; PARASITISM; SEXUAL SELECTION;

ACARI; DIPTERA; DROSOPHILA NIGROSPIRACULA; DROSOPHILIDAE; MACROCHELES SUBBADIUS;

EID: 0030620328     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/286032     Document Type: Article

References (84)

1. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, N.J.
2. Arnold, S. J., and M. J. Wade. 1984. On the measurement of natural selection: applications. Evolution 38:720-734.
3. Baker, N. E., M. Mlodzik, and G. M. Rubin. 1990. Spacing differentiation in the developing Drosophila eye: a fibrinogen-related lateral inhibitor encoded by scabrous. Science (Washington, D.C.) 250:1370-1377.
4. Biémont, C. 1983. Homeostasis, enzymatic heterozygosity and inbreeding depression in natural populations of Drosophila melanogaster. Genetica 61:179-189.
5. Charlesworth, D., and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18:237-268.
6. Clarke, G. M. 1993. Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality. Environmental Pollution 82:207-211.
7. Clarke, G. M., and J. A. McKenzie. 1987. Developmental stability of insecticide resistant phenotypes in blowfly: a result of canalizing natural selection. Nature (London) 325:345-346.
8. Festa-Bianchet, M. 1988. Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Animal Behaviour 36:1445-1454.
9. Fields, S. J., M. Spiers, I. Hershkovitz, and G. Livshits. 1995. Reliability of reliability coefficients in the estimation of asymmetry. American Journal of Physical Anthropology 96:83-87.
10. Fowler, K., and M. C. Whitlock. 1994. Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity 73:373-376.
11. Graham, J. H., and J. D. Felley. 1985. Genomic coadaptation and developmental stability within introgressed populations of Enneacanthus gloriousus and E. obesus (Pisces, Centrarchidae). Evolution 39:104-114.
12. Grammer, K., and R. Thornhill. 1994. Human (Homo sapiens) facial attractiveness and sexual selection: the role of symmetry and averageness. Journal of Comparative Psychology 108:233-242.
13. Heed, W. D. 1978. Ecology and genetics of Sonoran desert Drosophila. Pages 109-126 in P. Brussard, ed. Ecological genetics: the interface. Springer, New York.
14. Karney, W. W., and M. T. Tong. 1972. Malabsorption in Plasmodium flaciparum malaria. American Journal of Tropical Medicine and Hygiene 21:1-5.
15. Krantz, G. W. 1983. Mites as biological control agents of dung-breeding flies, with special reference to the Macrochelidae. Pages 91-98 in M. A. Hoy, G. L. Cunningham, and L. Knutson, eds. Biological control of pests by mites. University of California special publication 3304. University of California, Berkeley.
16. Leary, R. F., and F. W. Allendorf. 1989. Fluctuating asymmetry as an indicator of stress: implications for conservation biology. Trends in Ecology & Evolution 4:214-217.
17. Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1983. Developmental stability and enzyme heterozygosity in rainbow trout. Nature (London) 301:71-72.
18. _. 1984. Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. American Naturalist 124:540-551.
19. Liggett, A. C., I. F. Harvey, and J. T. Manning. 1993. Fluctuating asymmetry in Scathophaga stercoraria L.: successful males are more symmetrical. Animal Behaviour 45:1041-1043.
20. Livshits, G., and E. Kobyliansky. 1989. Study of genetic variance in fluctuating asymmetry of anthropometrical traits. Annals of Human Biology 116:121-129.
21. Livshits, G., L. Davidi, E. Kobyliansky, D. Ben-Amitai, Y. Levi, and P. Merlob. 1988. Decreased developmental stability as assessed by fluctuating asymmetry of morphometric traits in preterm infants. American Journal of Medical Genetics 29:793-805.
22. Markow, T. A. 1987. Genetic and sensory basis of sexual selection in Drosophila. Pages 89-95 in M. D. Huettel, ed. Evolutionary genetics of invertebrate behavior. Plenum, New York.
23. _. 1988. Reproductive behavior of Drosophila melanogaster and D. nigrospiracula in the field and in the laboratory. Journal of Comparative Psychology 102:169-173.
24. _. 1995. Evolutionary ecology of developmental instability. Annual Review of Entomology 40: 105-120.
25. Markow, T. A., and J. F. Martin. 1993. Inbreeding and developmental stability in a small human population. Annals of Human Biology 20:389-394.
26. Markow, T. A., and J. P. Ricker. 1991. Developmental stability in hybrids between the sibling species pair, Drosophila melanogaster and Drosophila simulans. Genetica 84:115-121.
27. _. 1992. Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity 69:122-127.
28. Mather, K. 1953. Genetical control of stability in development. Heredity 7:297-336.
29. McGregor, I. A. 1987. The significance of parasitic infections in terms of clinical disease: a personal view. Parasitology 94:5159-5178.
30. Møller, A. P. 1991. Parasites, sexual ornaments, and mate choice in the barn swallow. Pages 328-343 in J. E. Loye and M. Zuk, eds. Bird-parasite interactions. Oxford University Press, Oxford.
31. _. 1992a. Female swallow preference for symmetrical male sexual ornaments. Nature (London) 357:238-240.
32. _. 1992b. Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters. Journal of Evolutionary Biology 5:691-699.
33. _. 1993. Female preference for apparently symmetrical male sexual ornaments in the barn swallow Hirundo rustica. Behavioral Ecology and Sociobiology 32:371-376.
34. _. 1994. Sexual selection in the barn swallow (Hirundo rustica). IV. Patterns of fluctuating asymmetry and selection against asymmetry. Evolution 48:658-670.
35. _. 1996. Sexual selection, viability selection, and developmental stability in the domestic fly Musca domestica. Evolution 50:746-752.
36. Naugler, C. T., and S. M. Leech. 1994. Fluctuating asymmetry and survival ability in the forest tent caterpillar moth Malacosoma disstria: implications for pest management. Entomologia Experimentalis et Applicata 70:295-298.
37. Neter, J., W. Wasserman, and M. H. Kutner. 1990. Applied linear statistical models. Irwin, Homewood, Ill.
38. Newell-Morris, L. L., C. E. Fahrenbruch, and G. P. Sackett. 1989. Prenatal psychological stress, dermatogliphic asymmetry and pregnancy outcome in the pigtailed macaque (Macaca nemestrina). Biology of the Neonate 56:61-75.
39. Packer, C., and A. E. Pusey. 1993. Should a lion change its spots? Nature (London) 363:695.
40. Palmer, A. R. 1994. Fluctuating asymmetry analyses: a primer. Pages 335-364 in T. A. Markow, ed. Developmental instability: its origins and evolutionary implications. Kluwer, Norwell.
41. Palmer, A. R., and C. Strobeck. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics 17:391-421.
42. _. 1992. Fluctuating asymmetry as a measure of developmental stability: implications of nonnormal distributions and power of statistical tests. Acta Zoologica Fennica 191:57-72.
43. Parsons, P. A. 1962. Maternal age and developmental variability. Journal of Experimental Biology 39: 251-260.
44. _. 1990. Fluctuating asymmetry: an epigenic measure of stress. Biological Reviews 65:131-145.
45. Pereira, C., and M. P. de Castro. 1945. Contribuiçao para o conhecimento da especie tipo de Macrocheles Latr. (Acarina): M. muscaedomesticae (Scopoli, 1772). Arquivos do Instituto Biologico, São Paulo 16:153-156.
46. Poinar, G. O., Jr. 1983. The natural history of nematodes. Prentice Hall, Upper Saddle River, N.J.
47. Polak, M. 1993. Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: implications for sexual selection. Genetica 89:255-265.
48. _. 1996. Ectoparasitic effects on host survival and reproduction: the Drosophila-Macrocheles association. Ecology 77:1379-1389.
49. _. 1997. Parasites, fluctuating asymmetry and sexual selection. In N. Beckage, ed. Parasites: effects on host hormones and behavior. Chapman & Hall, New York (in press).
50. Polak, M., and T. A. Markow. 1995. Effect of ectoparasitic mites on sexual selection in a Sonoran desert fruit fly. Evolution 49:660-669.
51. Polak, M., and R. Trivers. 1994. The science of symmetry in biology. Trends in Ecology & Evolution 9:122-124.
52. Posakony, J. W. 1994. Nature versus nurture: asymmetric cell divisions ;in Drosophila bristle development. Cell 76:415-418.
53. Radesäter, T., and H. Halldórsdóttir. 1993. Fluctuating asymmetry and forceps size in earwigs, Forficula auricularia. Animal Behaviour 45:626-628.
54. Rails, K., J. Ballou, and A. Templeton. 1988. Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology 2:185-193.
55. Reeve, E. C. R. 1960. Some genetic tests on asymmetry of sternopleural chaeta number in Drosophila. Genetic Research 1:151-172.
56. Robertson, F. S., and E. Reeve. 1952. Studies in quantitative inheritance. I. The effects of selection of wing and thorax length in Drosophila melanogaster. Journal of Genetics 50:414-448.
57. Rodriguez, J. G., C. F. Wade, and C. N. Wells. 1962. Nematodes as a natural food for Macrocheles muscaedomesticae (Acarina: Macrochelidae), a predator of the house fly egg. Annals of the Entomological Society of America 55:507-511.
58. Royce, L. A., and G. W. Krantz. 1991. A new rearing method for nematophagous mites. Pages 619-622 in F. Dusbábek and V. Bukva, eds. Modern acarology. Academia, Prague.
59. Sang, J. H. 1956. The quantitative nutritional requirements of Drosophila melanogaster. Journal of Experimental Biology 33:45-72.
60. SAS. 1989. SAS user's guide: statistics. Version 5. SAS Institute, Cary, N.C.
61. Sciulli, P. W., W. J. Doyle, C. Kelley, P. Siegel, and M. I. Siegel. 1979. The interaction of Stressors in the induction of increased levels of fluctuating asymmetry in the laboratory rat. American Journal of Physical Anthropology 50:279-284.
62. Siegel, M. I., and H. H. Smookler. 1973. Fluctuating dental asymmetry and audiogenic stress. Growth 37:35-39.
63. Simpson, P. 1990. Lateral inhibition and the development of the sensory bristles of the adult peripheral nervous system of Drosophila. Development 109:509-519.
64. Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman, New York.
65. Swaddle, J. P., and I. C. Cuthill. 1994a. Female zebra finches prefer males with symmetric chest plum-age. Proceedings of the Royal Society of London B, Biological Sciences 258:267-271.
66. _. 1994b. Preference for symmetric males by female zebra finches. Nature (London) 367:165-166.
67. _. 1995. Asymmetry and human facial attractiveness: symmetry may not always be beautiful. Proceedings of the Royal Society of London B, Biological Sciences 261:111-116.
68. Tanaka, S. 1982. Variations in nine-spine stickelbacks, Pungitius pungitius and P. sinensis, in Honsu. Japanese Journal of Ichthyology 29:203-212.
69. Thoday, J. M. 1958. Homeostasis in a selection experiment. Heredity 12:401-415.
70. Thompson, S. N. 1983. Biochemical and physiological effects of metazoan endoparasites on their host species. Comparative Biochemistry and Physiology B, Comparative Biochemistry 74:183-211.
71. Thornhill, R. 1992a. Female preference for the pheromone of males with low fluctuating asymmetry in the Japanese scorpionfly (Panorpa japonica: Mecoptera). Behavioral Ecology 3:277-283.
72. _. 1992b. Fluctuating asymmetry and the mating system of the Japanese scorpionfly, Panorpa japonica. Animal Behaviour 44:867-879.
73. Thornhill, R., and J. Alcock. 1983. The evolution of insect mating systems. Harvard University Press, Cambridge, Mass.
74. Thornhill, R., and P. Sauer. 1992. Genetic sire effects on the fighting ability of sons and daughters and mating success of sons in a scorpionfly. Animal Behaviour 43:225-264.
75. Van Valen, L. 1962. A study of fluctuating asymmetry. Evolution 16:125-142.
76. Waddington, C. H. 1957. The strategy of the genes. Allen & Unwin, London.
77. Wakefield, J., K. Harris, and T. A. Markow. 1993. Parental age and developmental stability in Drosophila melanogaster. Genetica 89:235-244.
78. Wakelin, D. 1978. Genetic control of susceptibility and resistance to parasitic infection. Advances in Parasitology 16:219-308.
79. _. 1985. Genetic control of immunity to helminth infections. Parasitology Today 1:17-23.
80. Wakelin, D., and J. M. Blackwell. 1988. Genetics of resistance to bacterial and parasitic infection. Taylor & Francis, London.
81. Warrell, D. A. 1987. Pathophysiology of severe falciparum malaria in man. Parasitology 94:553-576.
82. Welch, H. E. 1959. Taxonomy, life cycle, development, and habits of two new species of Allantonematidae (Nematoda) parasitic in drosophilid flies. Parasitology 49:83-103.
83. Whitefield, P. J. 1979. The biology of parasitism: an introduction to the study of associating organisms. University Park Press, Baltimore.
84. Wilber, E., L. Newell-Morris, and A. Pytkowicz Streissguth. 1993. Dermatoglyphic asymmetry in fetal alcohol syndrome. Biology of the Neonate 64:1-6.