A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: Fluctuating asymmetry as an indicator of reproductive and genetic stress

Proceedings of the Royal Society B: Biological Sciences

Volumn 267, Issue 1446, 2000, Pages 875-882

  Gomendio, M ^a   Cassinello, J ^a   Roldan, E R S ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Ejaculate; Fluctuating asymmetry; Gazelles; Inbreeding; Spermatozoa; Ungulate

Indexed keywords

ENDANGERED SPECIES; FLUCTUATING ASYMMETRY; INBREEDING; STRESS; UNGULATE;

ANIMAL BEHAVIOR; ARTICLE; EJACULATION; FEMALE; INBREEDING; MALE; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; UNGULATE;

GAZELLA CUVIERI; GAZELLA DAMA; GAZELLES DORCAS;

EID: 0034616504     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2000.1084     Document Type: Article

References (72)

1. Alados, C. L., Escós, J. & Vericad, J. R. 1988 Captive populations of Northwest African Antilopinae and Caprinac at the Estación Experimental de Zonas Aridas. In Conservation and biology of desert antelopes (ed. A. Dixon & D. Jones), pp. 199-211. Bromley, Kent: Christopher Helm.
2. Allendorf, F. W. & Leary, R. F. 1986 Heterozygosity and fitness in natural populations of animals. In Conservation biology. The science of scarcity and diversity (ed. M. E. Soulé), pp. 57-76. Sunderland, MA: Sinauer Associates.
3. Ballou, J. 1983 Calculating inbreeding coefficients from pedigrees. In Genetics and conservation: a reference for managing wild animal and plant populations (ed. C. M. Schonewald-Cox, S. M. Chambers, B. MacBryde & L. Thomas), pp. 509-520. London: Benjamin/Cummins Publishing Co.
4. Bensch, S., Hasselquist, D. & Von Schantz, T. 1994 Genetic similarity between parents predicts hatching failure: nonincestuous inbreeding in the great reed warbler? Evolution 48, 317-326.
5. Birkhead, T. R. & Moller, A. P. (ed.) 1998 Sperm competition and sexual selection. London: Academic Press.
6. Caro, T. M. & Laurenson, M. K. 1994 Ecological and genetic factors in conservation: a cautionary tale. Science 263, 485-486.
7. Cassinello, J., Abaigar, T., Gomendio, M. & Roldan, E. R. S. 1998 Characteristics of the ejaculate in three endangered species of gazelles (Gazella dama mhorr, G. dorcas neglecta and G. cuvieri). J. Reprod. Fert. 113, 35-45.
8. Caughley, G. 1994 Directions in conservation biology. J. Anim. Ecol. 63, 215-244.
9. Charlesworlh, D. & Charlesworth, B. 1987 Inbreeding depression and its evolutionary consequences. A. Rev. Ecol. Syst. 18, 237-268.
10. Clarke, G. M. 1998 Developmental stability and fitness: the evidence is not quite so clear. Am. Nat. 152, 762-766.
11. Coltman, D. W., Bowen, W. D. & Wright, J. M. 1998 Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B 265, 803-809.
12. Coulson, T. N., Pemberton, J. M., Albon, S. D., Beaumont, M., Marshall, T. C., Slate, J., Guinness, F. E. & Clutton-Brock, T. H. 1998 Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B 265, 489-495.
13. Crow, J. F. 1997 The high spontaneous mutation rate: is it a health risk? Proc. Natl Acad. Sci. USA 94, 8380-8386.
14. Donnelly, E. T., Lewis, S. E. M., McNally, J. A. & Thompson, W. 1998 In vitro fertilization and pregnancy rates: the influence of sperm motility and morphology on IVF outcome. Fertil. Steril. 70, 305-314.
15. Dudash, M. R. & Carr, D. E. 1998 Genetics underlying inbreeding depression in Mimulus with contrasting mating systems. Nature 393, 682-684.
16. Eggertkruse, W., Schwarz, H., Rohr, G., Demirakca, T., Tilgen, W. & Runnebaum, B. 1996 Sperm morphology assessment using strict criteria and male fertility under in vivo conditions of conception. Hum. Reprod. 11, 139-146.
17. Eldridge, M. D. B., King, J. M., Loupis, A. K., Spencer, P. B. S., Taylor, A. C., Pope, L. C. & Hall, G. P. 1999 Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Conserv. Biol. 13, 531-541.
18. Frankham, R. 1995a Conservation genetics. A. Rev. Genet. 29, 305-327.
19. Frankham, R. 1995b Inbreeding and extinction: a threshold effect. Conserv. Biol. 9, 792-799.
20. Gibbs, H. L. & Grant, P. R. 1989 Inbreeding in Darwin's medium ground finches (Geospizafortis). Evolution 43, 1273-1284.
21. Gomendio, M. & Roldan, E. R. S. 1993 Coevolution between male ejaculates and female reproductive biology in eutherian mammals. Proc. R. Soc. Lond. B 252, 7-12.
22. Gomendio, M., Harcourt, A. H. & Roldan, E. R. S. 1998 Sperm competition in mammals. In Sperm competition and sexual selection (ed. T. R. Birkhead & A. P. Moller), pp. 667 751. London: Academic Press.
23. Grant, P. R. & Grant, B. R. 1995 The founding of a new population of Darwin's finches. Evolution 49, 229-240.
24. Harcourt, A. H. 1991 Endangered species. Nature 354, 10.
25. Hoogland, J. L. 1992 Levels of inbreeding among prairie dogs. Am. Nat. 139, 591-602.
26. Jimenez, J. A., Hughes, K. A., Alaks, G., Graham, L. & Lacy, R. C. 1994 An experimental study of inbreeding depression in a natural habitat. Science 266, 271-273.
27. Keller, L. F. 1998 Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52, 240-250.
28. Keller, L. F., Arcese, P., Smith, J. N. M., Hochachka, W. M. & Stearns, S. C. 1994 Selection against inbred song sparrows during a natural population bottleneck. Nature 372, 356-357.
29. Kempenaers, B., Adriaensen, F., Van Noordwijk, A. J. & Dhont, A. A. 1996 Genetic similarity, inbreeding and hatching failure in blue tits: are unhatched eggs infertile? Proc. R. Soc. Lond. B 263, 179-185.
30. Lacy, R. C., Alaks, G. & Walsh, A. 1996 Hierarchical analysis of inbreeding depression in Peromyscus polionotus. Evolution 50, 2187-2200.
31. Lande, R. 1988 Genetics and demography in biological conservation. Science 241, 1455-1460.
32. Lande, R. 1993 Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142, 911-927.
33. Lerner, I. M. 1954 Genetic homeostasis. Edinburgh: Oliver & Boyd.
34. Madsen, T., Shine, R., Olsson, M. & Wittzell, H. 1999 Restoration of an inbred adder population. Nature 402, 34-35.
35. Margulis, S. W. & Altman, J. A. 1997 Behavioural risk factors in the reproduction of inbred and outbred Oldfield mice. Anim. Behav. 54, 397-408.
36. Markow, T. A. 1995 Evolutionary ecology and developmental instability. A. Rev. Entomol. 40, 105-120.
37. Matthews, I. M., Evans, J. P. & Magurran, A. E. 1997 Male display rate reveals ejaculate characteristics in theTrinidadian guppy Poecilia reticulata. Proc. R. Soc. Lond. B 264, 695-700.
38. Menotti-Raymond, M. & O'Brien, S. J. 1993 Dating the genetic bottleneck of the African cheetah. Proc. Natl Acad. Sci. USA 90, 3172-3176.
39. Mills, L. S. & Smouse, P. E. 1994 Demographic consequences of inbreeding in remnant populations. Am. Nat. 144, 412-431.
40. Mitton, J. B. 1993 Theory and data pertinent to the relationship between heterozygosity and fitness. In The natural history of inbreeding and outbreeding (ed. N. W. Thornhill), pp. 17-41. University of Chicago Press.
41. Moller, A. P. 1999 Developmental stability is related to fitness. Am. Nat. 153, 556-560.
42. Moller, A. P. & Swaddle, J. P. 1997 Developmental stability and evolution. Oxford University Press.
43. Moller, A. P. & Thornhill, R. 1998 Bilateral symmetry and sexual selection: a meta-analysis. Am. Nat. 151, 174-192.
44. O'Brien, S. J., Wildt, D. E., Goldman, D., Merril, C. R. & Bush, M. 1983 The cheetah is depauperate in genetic variation. Science 221, 459-462.
45. O'Brien, S. J., Roelke, M. E., Newman, A., Winkler, C. A., Meltzer, D., Colly, L., Everman, J. F., Bush, M. & Wildt, D. E. 1985 Genetic basis for species vulnerability in the cheetah. Science 227, 1428-1434.
46. O'Brien, S. J., Wildt, D. E., Bush, M., Caro, T. M., FitzGibbon, C., Aggundey, I. & Leakey, R. E. 1987 East African cheetahs: evidence for two population bottlenecks? Proc. Natl Acad. Sci. USA 84, 508-511.
47. Olmedo, G., Escos, J. & Gomendio, M. 1985 Reproduction de Gazella cuvieri en captivité. Mammalia 49, 501-507.
48. Palmer, A. R. & Strobeck, C. 1986 Fluctuating asymmetry: measurement, analysis, patterns. A. Rev. Ecol. Syst. 17, 391-421.
49. Parsons, P. A. 1990 Fluctuating asymmetry: an epigenetic measure of stress. Biol. Rev. 65, 131-145.
50. Parsons, P. A. 1992 Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68, 361-364.
51. Parsons, P. A. 1996 Conservation strategies: adaptation to stress and the preservation of genetic diversity. Biol. J. Linn. Soc. 58, 471-482.
52. Quattro, J. M. & Vrijenhoek, R. C. 1989 Fitness differences among remnant populations of the endangered Sonoran topminnow. Science 245, 976-978.
53. Ralls, K., Brugger, K. & Ballou, J. 1979 Inbreeding and juvenile mortality in small populations of ungulates. Science 206, 1101-1103.
54. Roldan, E. R. S., Cassinello, J., Abaigar. T. & Gomendio, M. 1998 Inbreeding, fluctuating asymmetry and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B 265, 243-248.
55. Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W. & Hanski, I. 1998 Inbreeding and extinction in a butterfly metapopulation. Nature 392, 491-494.
56. Sheldon, B. C. 1994 Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc. R. Soc. Lond. B 257, 25-30.
57. Sheridan, L. & Pomiankowski, A. 1997 Fluctuating asymmetry, spot asymmetry and inbreeding depression in the sexual coloration of the male guppy fish. Heredity 79, 515-523.
58. Shields, W. M. 1993 The natural and unnatural history of inbreeding and outbreeding. In The natural history of inbreeding and outbreeding (ed. N. W. Thornhill), pp. 143-169. University of Chicago Press.
59. Short, R. V. 1997 The testis: the witness of the mating system, the site of mutation and the engine of desire. Acta Pediatr. (Suppl.) 422, 3-7.
60. Smith, M. H., Chesser, R. K., Cothran, E. G. & Johns, P. E. 1982 Genetic variability and antler growth in a natural population of white-tailed deer. In Antler development in the Cervidae (ed. R. D. Brown), pp. 365-368. Kingsville, TX: Caesar Klerberg Wildlife Research Institute.
61. Soderquist, L., Janson, L., Larsson, K. & Einarsson, S. 1991 Sperm morphology and fertility in AI bulls. J. Vet. Med. Assoc. 38, 534-343.
62. Stockley, P., Searle, J. B., MacDonald, D.W. & Jones, C. S. 1993 Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc. R. Soc. Lond. B 254, 173 179.
63. Swaddle, J. P. 1999a Limits to length asymmetry detection in starlings: implications for biological signalling. Proc. R. Soc. Lond. B 266, 1299-1303.
64. Swaddle, J. P. 1999b Visual signalling by asymmetry: a review of perceptual processes. Phil. Trans. R. Soc. Lond. B 354, 1383-1393.
65. Tamuli, M. K. & Watson, P. F. 1994 Use of a simple staining technique to distinguish acrosomal changes in the live sperm sub-population. Anim. Reprod. Sci. 35, 247-254.
66. Thornhill, N. W. (ed.) 1993 The natural history of inbreeding and outbreeding. University of Chicago Press.
67. Van Noordwijk, A. J. & Scharloo, W. 1981 Inbreeding in an island population of the great tit. Evolution 35, 674-688.
68. Van Valen, L. 1962 Study of fluctuating asymmetry. Evolution 16, 125-142.
69. Wildt, D. E., Bush, M., Howard, J. G., O'Brien, S. J., Meltzer, D., Van Dyk, A., Ebedes, H. & Brand, D. J. 1983 Unique seminal quality in the South African cheetah and a comparative evaluation in the domestic cat. Biol. Reprod. 29, 1019-1025.
70. Wildt, D. E., O'Brien, S. J., Howard, J. G., Caro, T. M., Roelke, M. E., Brown, J. L. & Bush, M. 1987 Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of two subspecies. Biol. Reprod. 36, 351-360.
71. Wright, S. 1922 Coefficients of inbreeding and relationship. Am. Nat. 56, 330-338.
72. Zar, J. H. 1984 Biostatistical analysis, 2nd edn. Englewood Cliffs, NJ: Prentice-Hall.