Absence of male reproductive skew, along with high frequency of polyandry and conspecific brood parasitism in the lekking Houbara bustard Chlamydotis undulata undulata

Journal of Avian Biology

Volumn 41, Issue 2, 2010, Pages 117-127

  Lesobre, Loïc ^a   Lacroix, Frédéric ^a   Le Nuz, Eric ^a   Hingrat, Yves ^a   Chalah, Toni ^a   Jaime, Michel Saint ^b  

^a Emirates Center for Wildlife Propagation (ECWP)   (Morocco)

^b CP51   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BROOD PARASITISM; CONSPECIFIC; ENDANGERED SPECIES; FECUNDITY; GAMEBIRD; GENETIC MARKER; LEK; MALE BEHAVIOR; MATE CHOICE; PATERNITY; POLYANDRY; REPRODUCTIVE COST; REPRODUCTIVE STRATEGY; SPERM COMPETITION;

MOROCCO;

CHLAMYDOTIS UNDULATA UNDULATA;

EID: 77953350620     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.1600-048X.2009.04794.x     Document Type: Article

References (96)

1. Alatalo R V, Burke T, Dann J, Hanotte O, Höglund J, Lundberg A, Moss R, Rintamäki P T. Paternity, copulation disturbance and female choice in lekking black grouse. Anim. Behav 1996, 52:861-873.
2. Alatalo R V, Höglund J, Lundberg A, Sutherland W J. Evolution of black grouse leks: female preferences benefit males in larger leks. Behav. Ecol 1992, 3:53-59.
3. Andersson M, Simmons L W. Sexual selection and mate choice. Trends Ecol. Evol 2006, 21:296-302.
4. Apollonio M, Festa-Bianchet M, Mari F, Mattioli S, Sarno B. To lek or not to lek: mating strategies of male fallow deer. Behav. Ecol 1992, 3:25-31.
5. Arnold K E, Owens I P F. Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc. R. Soc. B 2002, 269:1263-1269.
6. Ballou J D, Lacy R C. Identifying genetically important individuals for management of genetic variation in pedigreed populations. Population management for survival and recovery. Analytical methods and strategies in small population conservation 1995, 76-111. Ballou J D, Gilpin MFoose T. Columbia Univ. Press
7. Beehler B M, Foster M S. Hotshots, hotspots and female preference in the organization of lek mating systems. Am. Nat 1988, 131:203-219.
8. Birkhead T R. Sperm competition in birds. Rev. Reprod 1998, 3:123-129.
9. Birkhead T R, Atkin L, Møller A P. Copulation behaviour of birds. Behaviour 1987, 101:101-138.
10. Birkhead T R, Møller A P. Sperm competition in birds: evolutionary causes and consequences 1992, Academic Press
11. Blouin M S. DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol. Evol 2003, 18:503-511.
12. Blouin M S, Parsons M, Lacaille V, Lotz S. Use of microsatellite loci to classify individuals by relatedness. Mol. Ecol 1996, 5:393-401.
13. Blumstein D T. Female preferences and effective population size. Anim. Conserv 1998, 1:173-177.
14. Bradbury J W, Gibson R M. Leks and mate choice. Mate choice 1983, 109-138. Bateson P, Cambridge Univ. Press
15. Bradbury J W, Gibson R M, Tsai I M. Hotspots and the dispersion of leks. Anim. Behav 1986, 34:1694-1709.
16. Brown B L, Gunter T P, Waters J M, Epifanio J M. Evaluating genetic diversity associated with propagation-assisted restoration of American Shad. Conserv. Biol 2000, 14:294-303.
17. Butler K, Field C, Herbinger C M, Smith B R. Accuracy, efficiency and robustness of four algorithms allowing full sibship reconstruction from DNA marker data. Mol. Ecol 2004, 13:1589-1600.
18. Charmantier A, Blondel J, Perret P, Lambrechts M M. Do extra-pair paternities provide genetic benefits for female blue tits Parus caeruleus? J. Avian Biol 2004, 35:524-532.
19. Chbel F, Broderick D, Idaghdour Y, Korrida A, McCormick P. Characterization of 22 microsatellites loci from the endangered Houbara bustard (Chlamydotis undulata undulata). Mol. Ecol. Notes 2002, 2:484-487.
20. Colegrave N, Kotiaho J S, Tomkins J L. Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evol. Ecol. Res 2002, 4:911-917.
21. Combreau O, Qiao J, Lawrence M, Gao X, Yao J, Yang W, Launay F. Breeding success in a Houbara bustard Chlamydotis [undulata] macqueenii population on the eastern fringe of the Jungar Basin, People's Republic of China. Ibis 2002, 144:E45-E56.
22. Crow J F, Kimura M. An introduction to population genetics theory 1970, Harper and Row Publ, New-York
23. Durães R, Loiselle B A, Parker P G, Blake J G. Female mate choice across spatial scales: influence of lek and male attributes on mating success of blue-crowned manakins. Proc. R. Soc. B 2009, 276:1875-1881.
24. Fiske P, Rintamäki P T, Karvonen E. Mating success in lekking males: a meta-analysis. Behav. Ecol 1998, 9:328-338.
25. Focardi S, Tinelli A. May random processes explain mating success in leks? Behav. Process 1996, 36:227-237.
26. Foster M S. Disruption, dispersion, and dominance in lek-breeding birds. Am. Nat 1983, 122:53-72.
27. Frankham R. Genetics and extinction. Biol. Conserv 2005, 126:131-140.
28. Gaucher P. Breeding biology of the Houbara bustard Chlamydotis undulata undulata in Algeria. Alauda 1995, 63:291-298.
29. Goodnight K F, Queller D C. Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol. Ecol 1999, 8:1231-1234.
30. Goriup P D. The world status of the Houbara bustard Chlamydotis undulata. Bird Conserv. Int 1997, 7:373-397.
31. Hardy O J, Vekemans X. SpageDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2002, 2:618-620.
32. Hayes S A, Costa D P, Harvey J T, Le Boeuf B J. Aquatic mating strategies of the male Pacific harbour seal (Phoca vitulina richardii): are males defending the hotspot? Mar. Mamm. Sci 2004, 20:639-656.
33. Hingrat Y, Saint Jalme M. Mating system of the Houbara bustard Chlamydotis undulata undulata in eastern Morocco. Ardeola 2005, 52:91-102.
34. Hingrat Y, Saint Jalme M, Chalah T, Orhant N, Lacroix F. Environmental and social constraints on breeding sites selection. Does the exploded-lek and hotspot model apply to the Houbara bustard Chlamydotis undulata undulata? J. Avian Biol 2008, 39:393-404.
35. Hingrat Y, Saint Jalme M, Ysnel F, Lacroix F, Seabury J, Rautureau P. Relationships between home-range size, sex and season with reference to the mating system of the Houbara bustard Chlamydotis undulata undulata. Ibis 2004, 146:314-322.
36. Höglund J, Alatalo R V. Leks 1995, Princeton Univ. Press
37. Höglund J, Montgomerie R, Widemo F. Costs and consequences of variation in the size of ruff leks. Behav. Ecol. Sociobiol 1993, 32:31-39.
38. Höglund J, Piertney S B, Alatalo R V, Lindell J, Lundberg A, Rintamäki P T. Inbreeding depression and male fitness in black grouse. Proc. R. Soc. B 2002, 269:711-715.
39. Guidelines for Re-introductions. Prepared by the IUCN/SSC Re-introduction Specialist Group 1998, Gland, Switzerland, IUCN
40. Jennions M D, Petrie M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev 2000, 75:21-64.
41. Jiguet F, Arroyo B, Bretagnolle V. Lek mating systems: a case study in the little bustard Tetrax tetrax. Behav. Process 2000, 51:63-82.
42. Jiguet F, Jaulin S, Arroyo B. Resource defence on exploded leks: do male little bustards, T. tetrax, control resources for females? Anim. Behav 2002, 63:899-905.
43. Kalinowski S T, Taper M L, Marshall T C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol 2007, 16:1099-1106.
44. Kempenaers B, Dhondt A A. Why do females engage in extra-pair copulations? A review of hypotheses and their predictions. Belg. J. Zool 1993, 123:93-103.
45. Kokko H, Sutherland W J, Lindström J, Reynolds J D, MacKenzie A. Individual mating success, lek stability, and the neglected limitations of statistical power. Anim. Behav 1998, 56:755-762.
46. Konovalov D A, Heg D I K. A maximum-likelihood relatedness estimator allowing for negative relatedness values. Mol. Ecol. Resour 2008, 8:256-263.
47. Konovalov D A, Manning C, Henshaw M T. Kingroup: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Mol. Ecol. Notes 2004, 4:779-782.
48. Krokene C, Rigstad K, Dale M, Lifjeld J T. The function of extrapair paternity in blue tits and great tits: good genes or fertility insurance? Behav. Ecol 1998, 9:649-656.
49. Lacroix F. The Emirates center for wildlife propagation: developing a comprehensive strategy to secure a self sustaining population of Houbara bustards in eastern Morocco. Houbara News 2003, 5:2.
50. Lacy R C. Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv. Biol 1987, 1:143-157.
51. Lanctot R B, Scribner K T, Kempenaers B, Weatherhead P J. Lekking without a paradox in the buff-breasted sandpiper. Am. Nat 1997, 149:1051-1070.
52. Lank D B, Smith C M. Conditional lekking in ruff (Philomachus pugnax). Behav. Ecol. Sociobiol 1987, 20:137-145.
53. Lank D B, Smith C M, Hanotte O, Ohtonen A, Bailey S, Burke T. High frequency of polyandry in a lek mating system. Behav. Ecol 2002, 13:209-215.
54. Laska M S, Hutchins M, Sheppard C, Worth W, Hundgen K, Bruning D. Reproduction by captive unplumed male lesser bird of paradise Paradisaea minor: evidence for an alternative mating strategy? Emu 1992, 92:108-111.
55. Lebigre C, Alatalo R V, Siitari H, Parri S. Restrictive mating by females on black grouse leks. Mol. Ecol 2007, 16:4380-4389.
56. Lesobre L. Structure génétique des populations menacées d'outarde Houbara (Chlamydotis undulata undulata) au Maroc. Implications à la gestion d'un élevage conservatoire et au renforcement des populations. 2008, PhD thesis, Muséum National d'Histoire Naturelle Paris, France.
57. Lewin R. Hotshots, hotspots, and female preference. Science 1988, 240:1277-1278.
58. Li C C, Weeks D E, Chakravarti A. Similarity of DNA finger-prints due to chance and relatedness. Hum. Hered 1993, 43:45-52.
59. Loyau A, Saint Jalme M, Cagniant C, Sorci G. Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav. Ecol. Sociobiol 2005, 58:552-557.
60. Lynch M, Ritland K. Estimation of pairwise relatedness with molecular markers. Genetics 1999, 152:1753-1766.
61. Lyon B E. Conspecific brood parasitism as a flexible female reproductive tactic in American coots. Anim. Behav 1993, 46:911-928.
62. Marshall T C, Slate J, Kruuk L E B, Pemberton J M. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol 1998, 7:639-655.
63. Milligan B G. Maximum-likelihood estimation of relatedness. Genetics 2003, 163:1153-1167.
64. Møller A P. Frequency of female copulations with multiple males and sexual selection. Am. Nat 1992, 139:1089-1101.
65. Morales M, Alonso J C, Martín C, Martín E, Alonso J A. Male sexual display and attractiveness in the great bustard Otis tarda: the role of body condition. J. Ethol 2003, 21:51-56.
66. Neff B D, Pitcher T E. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol 2005, 14:19-38.
67. Oh K P, Badyaev A V. Adaptive genetic complementarity in mate choice coexists with selection for elaborate sexual traits. Proc. R. Soc. B 2006, 273:1913-1919.
68. Oring L. Avian mating systems. Avian biology 1982, 1-92. Framer D SKing J RParkes K C. Academic Press, New York
69. Petrie M, Hall M, Halliday T, Budgey h, Pierpoint C. Multiple mating in a lekking bird: why do peahens mate with more than one male and with the male more than once? Behav. Ecol. Sociobiol 1992, 31:349-358.
70. Petrie M, Kempenaers B. Extra-pair paternity in birds: explaining variation between species and populations. Trends Ecol. Evol 1998, 13:52-58.
71. Petrie M, Lipsitch M. Avian polygyny is most likely in populations with high variability in heritable male fitness. Proc. R. Soc. B 1994, 256:275-280.
72. Pitra C, D'Aloia M-A, Lieckfeldt D, Combreau O. Genetic variation across the current range of the Asian houbara bustard (Chlamydotis undulata macqueenii). Conserv. Genet 2004, 5:205-215.
73. Quader S. Mate choice and its implications for conservation and management. Curr. Sci. (Bangalore) 2005, 89:1220-1229.
74. Queller D C, Goodnight K F. Estimating relatedness using genetic markers. Evolution 1989, 43:258-275.
75. Rintamäki P T, Höglund J, Alatalo R V, Lundberg A. Correlates of male mating success on black grouse (Tetrao tetrix L.) leks. Ann. Zool. Fenn 2001, 38:99-109.
76. Ritland K. Marker-inferred relatedness as a tool for detecting heritability in nature. Mol. Ecol 2000, 9:1195-1204.
77. Robert A, Couvet D, Sarrazin F. Integration of demography and genetics in population restorations. Ecoscience 2007, 14:463-471.
78. Rousset F. Genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resour 2008, 8:103-106.
79. Rubenstein D I. On the evolution of alternative mating strategies Kings college sociobiology group. Current problems in sociobiology, Cambridge Univer. Press 1982, 65-100.
80. Russello M A, Amato G. Ex situ population management in the absence of pedigree information. Mol. Ecol 2004, 13:2829-2840.
81. Saint Jalme M, Gaucher P, Paillat P. Artificial insemination in Houbara bustards (Chlamydotis undulata): influence of the number of spermatozoa and insemination frequency on fertility and ability to hatch. J. Reprod. Fertil 1994, 100:93-103.
82. Saint Jalme M, Van Heezik Y. Propagation of the Houbara bustard 1996, Keegan Paul International, London
83. Schultz H, Seddon P J. Biology and Status of the Houbara bustard. Propagation of the Houbara bustard 1996, 3-14. Saint Jalme M, Van Heezik Y. Keegan Paul International, London
84. Seddon P J, Launay F, Van Heezik Y, Al Bowardi M. Methods for live trapping Houbara bustards. J. Field Ornithol 1999, 70:169-181.
85. Semple K, Wayne R K, Gibson R M. Microsatellite analysis of female mating behaviour in lek-breeding sage grouse. Mol. Ecol 2001, 10:2043-2048.
86. Shorey L. Mating success on white-bearded manakin (Manacus manacus) leks: male characteristics and relatedness. Behav. Ecol. Sociobiol 2002, 52:451-457.
87. Simmons L W. The evolution of polyandry. Annu. Rev. Ecol. Syst 2005, 36:125-146.
88. Stiver J R, Apa A D, Remington T E, Gibson R M. Polygyny and female breeding failure reduce effective population size in the lekking Gunnison sage-grouse. Biol. Conserv 2008, 141:472-481.
89. Tourenq C, Combreau O, Lawrence M, Pole S B, Spalton A, Xinji G, Al Baidani M, Launay F. Alarming Houbara bustard population trends in Asia. Biol. Conserv 2005, 121:1-8.
90. Tregenza T, Wedell N. Genetic compatibility, mate choice and patterns of parentage: invited Review. Mol. Ecol 2000, 9:1013-1027.
91. Van de Casteele T, Galbusera P, Matthysen E. A comparison of microsatellite-based pairwise relatedness estimators. Mol. Ecol 2001, 10:1539-1549.
92. van Heezik Y, Saint Jalme M, Seddon P J. Temperature and egg-laying experience influence breeding performance of captive female Houbara bustards. J. Avian Biol 2002, 33:63-70.
93. Wang J. An estimator for pairwise relatedness using molecular markers. Genetics 2002, 160:1203-1215.
94. Wiley R H. Lekking in birds and mammals: behavioral and evolutionary issues. Adv. Study Behav 1991, 20:201-291.
95. Yom Tov Y. An updated list and some comments on the occurrence of intraspecific nest parasitism in birds. Ibis 2001, 143:133-143.
96. Zeh J A, Zeh D W. Reproductive mode and the genetic benefits of polyandry. Anim. Behav 2001, 61:1051-1063.