Patterns of male reproductive success in a highly promiscuous whale species: The endangered North Atlantic right whale

Molecular Ecology

Volumn 16, Issue 24, 2007, Pages 5277-5293

  Frasier, T R ^a   Hamilton, P K ^b   Brown, M W ^b   Conger, L A ^b   Knowlton, A R ^b   Marx, M K ^b   Slay, C K ^b   Kraus, S D ^b   White, B N ^a  

^a TRENT UNIVERSITY   (Canada)

^b NEW ENGLAND AQUARIUM   (United States)

Author keywords

Endangered species; Mating systems; Paternity; Polygyny; Reproductive success; Right whale

Indexed keywords

AGING; ANIMAL; ARTICLE; ATLANTIC OCEAN; CLASSIFICATION; FEMALE; MALE; PHYSIOLOGY; POPULATION DENSITY; REPRODUCTION; SEXUAL BEHAVIOR; SPECIES EXTINCTION; TIME; WHALE;

AGING; ANIMALS; ATLANTIC OCEAN; EXTINCTION, BIOLOGICAL; FEMALE; MALE; POPULATION DENSITY; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL; TIME FACTORS; WHALES;

BALAENIDAE; CETACEA; EUBALAENA GLACIALIS; MAMMALIA; MYSTICETI;

EID: 37249022872     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2007.03570.x     Document Type: Article

References (94)

1. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity, 87, 257 265.
2. Amos W, Worthington Wilmer J, Kokko H (2001a) Do female grey seals select genetically diverse mates? Animal Behaviour, 62, 157 164.
3. Amos W, Worthington Wilmer J, Fullard K et al 2001b) The influence of parental relatedness on reproductive success. Proceedings of the Royal Society of London. Series B, Biological Sciences, 268, 2021 2027.
4. Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: theory. Evolution, 38, 709 719.
5. Atkinson S (2002) Male reproductive systems. In : Encyclopedia of Marine Mammals (eds Perrin WF, Würsig B, Thewissen JGM pp. 700 704. Academic Press, San Diego.
6. Best PB (1990) Natural markings and their use in determining calving intervals in right whales off South Africa. South African Journal of Zoology, 25, 114 123.
7. Best PB (1994) Seasonality of reproduction and the length of gestation in southern right whales Eubalaena australis. Journal of Zoology, 232, 175 189.
8. Best PB, Brandão A, Butterworth DS (2001) Demographic parameters of southern right whales off South Africa. Journal of Cetacean Research and Management (Special Issue), 2, 161 170.
9. Best PB, Schaeff CM, Reeb D, Palsbøll PJ (2003) Composition and possible function of social groupings of southern right whales in South African waters. Behaviour, 140, 1469 1494.
10. Boness DJ, Bowen WD, Francis JM (1993) Implications of DNA fingerprinting for mating systems and reproductive strategies of pinnipeds. Symposium of the Zoological Society of London, 66, 61 93.
11. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics, 32, 314 331.
12. Brown MW, Brault S, Hamilton PK et al 2001) Sighting heterogeneity of right whales in the western North Atlantic : 1980-1992. Journal of Cetacean Research and Management (Special Issue), 2, 245 250.
13. Brown MW, Kraus SD, Gaskin DE (1991) Reaction of North Atlantic right whales (Eubalaena glacialis) to skin biopsy sampling for genetic and pollutant analysis. Report of the International Whaling Commission, Special Issue, 13, 81 89.
14. Brown MW, Kraus SD, Gaskin DE, White BN (1994) Sexual composition and analysis of reproductive females in the North Atlantic right whale, Eubalaena glacialis, population. Marine Mammal Science, 10, 252 265.
15. Brown MW, Kraus SD, Slay CK, Garrison LP (2007) Surveying for discovery, science, and management. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 105 137. Harvard University Press, Cambridge, Massachusetts.
16. Brownell RL Jr., Ralls K (1986) Potential for sperm competition in baleen whales. Report of the International Whaling Commission, Special Issue, 8, 97 112.
17. Caswell H, Fujiwara M, Brault S (1999) Declining survival probability threatens the North Atlantic right whale. Proceedings of the National Academy of Sciences, USA, 96, 3308 3313.
18. Caughley G (1994) Directions in conservation biology. Journal of Animal Ecology, 63, 215 244.
19. Cerchio S, Jacobsen JK, Cholewiak DM, Falcone EA, Merriwether DA (2005) Paternity in humpback whales, Megaptera novaeangliae: assessing polygyny and skew in male reproductive success. Animal Behaviour, 70, 267 277.
20. Chakraborty R, Meagher TR, Smouse PE (1988) Parentage analysis with genetic markers in natural populations. I. The expected proportion of offspring with unambiguous paternity. Genetics, 118, 527 536.
21. Clapham PJ (1992) Age at attainment of sexual maturity in humpback whales, Megaptera novaeangliae. Canadian Journal of Zoology, 70, 1470 1472.
22. Clapham PJ (1996) The social and reproductive biology of humpback whales: an ecological perspective. Mammal Review, 26, 27 49.
23. Clapham PJ (2000) The humpback whale: seasonal feeding and breeding in a baleen whale. In : Cetacean Societies: Field Studies of Dolphins and Whales (eds Mann J, Connor RC, Tyack PL, Whitehead H pp. 173 196. University of Chicago Press, Chicago.
24. Clapham PJ, Palsbøll PJ (1997) Molecular analysis of paternity shows promiscuous mating in female humpback whales (Megaptera novaeangliae, Borowski). Proceedings of the Royal Society of London. Series B, Biological Sciences, 264, 95 98.
25. Clapham PJ, Young SB, Brownell RL Jr. (1999) Baleen whales: conservation issues and status of the most endangered populations. Mammal Review, 29, 35 60.
26. Clutton-Brock TH, Guiness FE, Albon SD (1982) Red Deer: Behavior and Ecology of Two Sexes. University of Chicago Press, Chicago.
27. Coltman DW, Bancroft DR, Robertson A, Smith JA, Clutton-Brock TH, Pemberton JM (1999b) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Molecular Ecology, 8, 1199 1209.
28. Coltman DW, Bowen WD, Wright JM (1998) Male mating success in an aquatically mating pinniped, the harbour seal (Phoca vitulina), assessed by microsatellite DNA markers. Molecular Ecology, 7, 627 638.
29. Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2002) Age-dependent sexual selection in bighorn rams. Proceedings of the Royal Society of London. Series B, Biological Sciences, 269, 165 172.
30. Coltman DW, Smith JA, Bancroft DR et al 1999a) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. American Naturalist, 154, 730 746.
31. Cooke JG, Rowntree VJ, Payne RS (2001) Estimates of demographic parameters for southern right whales (Eubalaena australis) observed off Península Valdés. Argentina. Journal of Cetacean Research and Management (Special Issue), 2, 125 132.
32. Daly M, Wilson M (1983) Sex, Evolution, and Behavior, 2nd edn. PWS Publishers, Belmont, California.
33. Darling JD, Bérubé M (2001) Interactions of singing humpback whales with other males. Marine Mammal Science, 17, 570 584.
34. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215 223.
35. Evett IW, Weir BS (1998) Interpreting DNA Evidence. Sinaur Associates, Sunderland, Massachusetts.
36. Feldhamer GA, Drickamer LC, Vessey SH, Merritt JF (1999) Mammalogy: Adaptation, Diversity, and Ecology. McGraw-Hill, Boston, Massachusetts.
37. Fisher RA (1958) The Genetical Theory of Natural Selection. Oxford University Press, Oxford, UK.
38. Frasier TR (2005) Integrating genetic and photo-identification data to assess reproductive success in the North Atlantic right whale (Eubalaena glacialis). PhD Thesis, McMaster University, Hamilton, Ontario.
39. Frasier TR, McLeod BA, Gillett RM, Brown MW, White BN (2007) Right whales past and present as revealed by their genes. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 200 231. Harvard University Press, Cambridge, Massachusetts.
40. Frasier TR, Rastogi T, Brown MW, Hamilton PK, Kraus SD, White BN (2006) Characterization of tetranucleotide microsatellite loci and development and validation of multiplex reactions for the study of right whale species (genus Eubalaena). Molecular Ecology Notes, 6, 1025 1029.
41. Fujiwara M, Caswell H (2001) Demography of the endangered North Atlantic right whale. Nature, 414, 537 541. 9.
42. Gibbs HL, Weatherhead PJ, Boag PT, White BN, Tabak LM, Hoysak DJ (1990) Realized reproductive success of polygynous red-winged blackbirds revealed by DNA markers. Science, 250, 1394 1397.
43. Ginsberg JR, Huck UW (1989) Sperm competition in mammals. Trends in Ecology & Evolution, 4, 74 79.
44. Ginsberg JR, Rubenstein DI (1990) Sperm competition and variation in zebra mating behavior. Behavioral Ecology and Sociobiology, 26, 427 434.
45. Gomendio M, Harcourt AH, Roldán ERS (1998) Sperm competition in mammals. In : Sperm Competition and Sexual Selection (eds Birkhead TR, Møller AP pp. 667 755. Academic Press, San Diego, California.
46. Halbert ND, Raudsepp T, Chowdhary BP, Derr JN (2004) Conservation genetic analysis of the Texas State Bison Herd. Journal of Mammalogy, 85, 924 931.
47. Hamilton PK, Knowlton AR, Marx MK, Kraus SD (1998) Age structure and longevity in North Atlantic right whales Eubalaena glacialis and their relation to reproduction. Marine Ecology Progress Series, 171, 285 292.
48. Hamilton PK, Marx MK, Kraus SD (1995) Weaning in North Atlantic right whales. Marine Mammal Science, 11, 386 390.
49. Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature, 293, 55 57.
50. Hayes SA, Pearse DE, Costa DP, Harvey JT, Le Boeuf BJ, Garza JC (2006) Mating systems and reproductive success in eastern Pacific harbour seals. Molecular Ecology, 15, 3023 3034.
51. Hoffman JI, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Molecular Ecology, 14, 599 612.
52. Holleley CE, Dickman CR, Crowther MS, Oldroyd BP (2006) Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Molecular Ecology, 15, 3439 3448.
53. Hughes CR (1998) Integrating molecular techniques with field methods in studies of social behavior: a revolution results. Ecology, 79, 383 399.
54. International Whaling Commission (2001) Report of the workshop on the status and trends of western North Atlantic right whales. Journal of Cetacean Research and Management (Special Issue), 2, 61 87.
55. Johnson AJ, Kraus SD, Kenney JF, Mayo CA (2007) The entangled lives of right whales and fishermen: can they coexist?. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 380 408. Harvard University Press, Cambridge, Massachusetts.
56. Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. Journal of Mammalogy, 67, 1 22.
57. Knowlton AR, Brown MW (2007) Running the gauntlet: right whales and vessel strikes. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 409 435. Harvard University Press, Cambridge, Massachusetts.
58. Knowlton AR, Kraus SD, Kenney RD (1994) Reproduction in North Atlantic right whales (Eubalaena glacialis). Canadian Journal of Zoology, 72, 1297 1305.
59. Kraus SD, Hamilton PK, Kenney RD, Knowlton AR, Slay CK (2001) Reproductive parameters of the North Atlantic right whale. Journal of Cetacean Research and Management (Special Issue), 2, 231 236.
60. Kraus SD, Hatch JJ (2001) Mating strategies in the North Atlantic right whale (Eubalaena glacialis). Journal of Cetacean Research and Management (Special Issue), 2, 237 244.
61. Kraus SD, Moore KE, Price CA et al 1986a) The use of photographs to identify individual North Atlantic right whales (Eubalaena glacialis). Report of the International Whaling Commission, Special Issue, 10, 145 151.
62. Kraus SD, Pace RM III, Frasier TR (2007) High investment, low return: the strange case of reproduction in Eubalaena glacialis. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 172 199. Harvard University Press, Cambridge, Massachusetts.
63. Kraus SD, Prescott JH, Knowlton AR, Stone GS (1986b) Migration and calving of right whales (Eubalaena glacialis) in the western North Atlantic. Report of the International Whaling Commission, Special Issue, 10, 139 144.
64. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7, 639 655.
65. Mate B, Duley P, Lagerquist B, Wenzel F, Stimpert A, Clapham P (2005) Observations of a female North Atlantic right whale (Eubalaena glacialis) in simultaneous copulation with two males: supporting evidence for sperm competition. Aquatic Mammals, 31, 157 160.
66. Menotti-Raymond M, O'Brien SJ (1995) Hypervariable genomic variation to reconstruct the natural history of populations: lessons from the big cats. Electrophoresis, 16, 1771 1774.
67. Moore MJ, McLellan WA, Daoust P-Y, Bonde RK, Knowlton AR (2007) Right whale mortality: a message from the dead to the living. In : The Urban Whale: North Atlantic Right Whales at the Crossroads (eds Kraus SD, Rolland RM pp. 358 379. Harvard University Press, Cambridge, Massachusetts.
68. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583 590.
69. Nielsen R, Mattila DK, Clapham PJ, Palsbøll PJ (2001) Statistical approaches to paternity analysis in natural populations and applications to the North Atlantic humpback whale. Genetics, 157, 1673 1682.
70. Ober C, Hyslop T, Elias S, Wiekamp LR, Hauck WW (1998) Human leukocyte antigen matching and fetal loss: results of a 10-year prospective study. Human Reproduction, 13, 33 38.
71. Pack AA, Salden DR, Ferrari MJ et al 1998) Male humpback whale dies in competitive group. Marine Mammal Science, 14, 861 873.
72. Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Molecular Ecology, 3, 487 495.
73. Parks SE (2003) Response of North Atlantic right whales (Eubalaena glacialis) to playback of calls recorded from surface active groups in both the North and South Atlantic. Marine Mammal Science, 19, 563 580.
74. Parks SE, Hamilton PK, Kraus SD, Tyack PL (2005) The gunshot sound produced by male North Atlantic right whales (Eubalaena glacialis) and its potential function in reproductive advertisement. Marine Mammal Science, 21, 458 475.
75. Payne R, Brazier O, Dorsey EM, Perkins JS, Rowntree VJ, Titus A (1983) External features in Southern right whales (Eubalaena australis) and their use in identifying individuals. In : Communication and Behaviour of Whales (ed. Payne R pp. 371 445. AAAS Selected Symposium 76. Westview Press, Boulder, Colorado.
76. Payne R, Dorsey EM (1983) Sexual dimorphism and aggressive use of callosities in right whales (Eubalaena australis). In : Communication and Behaviour of Whales (ed. Payne R pp. 295 329. AAAS Selected Symposium 76. Westview Press, Boulder.
77. Pemberton JM, Albon SD, Guiness FE, Clutton-Brock TH, Dover GA (1992) Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behavioral Ecology, 3, 66 75.
78. Pemberton JM, Coltman DW, Smith JA, Bancroft DR (2004) Mating patterns and male breeding success. In : Soay Sheep: Dynamics and Selection in an Island Population (eds Clutton-Brock T, Pemberton J pp. 166 189. Cambridge University Press, Cambridge, UK.
79. Pettis HM, Rolland RM, Hamilton PK, Brault S, Knowlton AR, Kraus SD (2004) Visual health assessment of North Atlantic right whales (Eubalaena glacialis) using photographs. Canadian Journal of Zoology, 82, 8 19.
80. Preston BT. Stevenson IR. Pemberton JM. Coltman DW. Wilson K (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proceedings of the Royal Society of London. Series B, Biological Sciences, 270, 633 640.
81. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution, 43, 258 275.
82. Quinn TW, Quinn JS, Cooke F, White BN (1987) DNA marker analysis detects multiple maternity and paternity in single broods of the lesser snow goose. Nature, 326, 392 394.
83. Rolland RM, Hunt KE, Kraus SD, Wasser SK (2005) Assessing reproductive status of right whale (Eubalaena glacialis) using fecal hormone metabolites. General and Comparative Endocrinology, 142, 308 317.
84. Rossiter SJ, Ransome RD, Faulkes CG, Dawson DA, Jones G (2006) Long-term paternity skew and the opportunity for sexual selection in a mammal with reversed secual size dimorphism. Molecular Ecology, 15, 3035 3043.
85. Shaw CN, Wilson PJ, White BN (2003) A reliable method of gender determination for mammals. Journal of Mammalogy, 84, 123 128.
86. Sironi M, Kraus SD, Nordheim EV, Rowntree VJ, Snowdon CT (2005) Age estimation of North Atlantic right whales (Eubalaena glacialis) by allometric measurements on photographs. Paper SC/57/BRG7 presented to the International Whaling Commission Scientific Committee, June 2005. 14pp.
87. Slate J, Marshall T, Pemberton J (2000) A retrospective assessment of the accuracy of the paternity inference program cervus. Molecular Ecology, 9, 801 808.
88. Taylor AC, Cowan PE, Fricke BL, Cooper DW (2000) Genetic analysis of the mating system of the common brushtail possum (Trichosurus vulpecula) in New Zealand farmland. Molecular Ecology, 9, 869 879.
89. Tyack PL (1981) Interactions between singing Hawaiian humpback whales and conspecifics nearby. Behavioral Ecology and Sociobiology, 8, 105 116.
90. Vigilant L, Hofreiter M, Seidel H, Boesch C (2001) Paternity and relatedness in wild chimpanzee communities. Proceedings of the National Academy of Sciences, USA, 98, 12890 12895.
91. Vilà C, Sundqvist A-K, Flagstad Ø et al 2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society of London, Series B, 270, 91 97.
92. Whitehead H, Payne R (1981) New techniques for assessing populations of right whales without killing them. In : Mammals in the Sea. Vol. III. FAO Fisheries Serial No. 5 eds Clark JG, Goodman J, Soave GA) pp. 189 209. United Nations Food and Agriculture Organization, Rome.
93. Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings of the Royal Society of London. Series B, Biological Sciences, 271, 819 826.
94. Worthington Wilmer J, Allen PJ, Pomeroy PP, Twiss SD, Amos W (1999) Where have all the fathers gone? An extensive microsatellite analysis of paternity in the grey seal (Halichoerus grypus). Molecular Ecology, 8, 1417 1429.