Polyandry as a mediator of sexual selection before and after mating

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1613, 2013, Pages

  Kvarnemo, Charlotta ^a,b   Simmons, Leigh W ^c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

Bateman gradient; Direct and indirect benefits; Mating competition; Sex roles; Sperm competition; Variation in reproductive success

Indexed keywords

COMPETITION (ECOLOGY); COPULATION; CRYPSIS; ESTIMATION METHOD; POLYANDRY; REPRODUCTION; SEXUAL SELECTION;

ANIMAL; BIOLOGICAL MODEL; COMPETITIVE BEHAVIOR; FEMALE; FERTILITY; GENETIC SELECTION; MALE; MATE CHOICE; PHYSIOLOGY; REVIEW; SEX RATIO; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; SPERMATOZOON;

ANIMALS; COMPETITIVE BEHAVIOR; FEMALE; FERTILITY; MALE; MATING PREFERENCE, ANIMAL; MODELS, BIOLOGICAL; SELECTION, GENETIC; SEX CHARACTERISTICS; SEX RATIO; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA;

MLCS; MLOWN;

EID: 84879475655     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0042     Document Type: Review

References (238)

1. Darwin C. 1871 The descent of man, and selection in relation to sex. London, UK: John Murray.
2. Bateman AJ. 1948 Intra-sexual selection in Drosophila. Heredity 2, 349-368. (doi:10.1038/ hdy.1948.21)
3. Trivers RL. 1972 Parental investment and sexual selection. In sexual selection and the descent of man, 1871-1971 (ed. BG Campbell), pp. 136-179. Chicago, IL: Aldine.
4. Emlen ST, Oring LW. 1977 Ecology, sexual selection, and the evolution of mating systems. Science 197, 215-223. (doi:10.1126/science.327542)
5. Clutton-Brock TH, Parker GA. 1992 Potential reproductive rates and the operation of sexual selection. Q. Rev. Biol. 67, 437-456. (doi:10.1086/417793)
6. Shuster SM, Wade MJ. 2003 Mating systems and strategies. Princeton, NJ: Princeton University Press.
7. Parker GA, Birkhead TR. 2013 Polyandry: the history of a revolution. Phil. Trans. R. Soc. B 368, 20120335. (doi:10.1098/rstb.2012.0335)
8. Shuster SM, Briggs WR, Dennis PA. 2013. How multiple mating by females affects sexual selection. Phil. Trans. R. Soc. B 368, 20120046. (doi:10.1098/ rstb.2012.0046)
9. Kvarnemo C, Ahnesjö I. 1996 The dynamics of operational sex ratios and competition for mates. Trends Ecol. Evol. 11, 404-408. (doi:10.1016/01695347(96)10056-2)
10. Ahnesjö I, Forsgren E, Kvarnemo C. 2008 Variation in sexual selection in fishes. In Fish behaviour (eds C Magnhagen, VA Braithwaite, E Forsgren, BG Kapoor), pp. 303-335. Enfield, NH: Science Publishers.
11. Kvarnemo C, Merilaita S. 2006 Mating distribution and its temporal dynamics affect operational sex ratio: a simulation study. Biol. J. Linn. Soc. 89, 551-559. (doi:10.1111/j.1095-8312.2006.00694.x)
12. Ahnesjö I, Kvarnemo C, Merilaita S. 2001 Using potential reproductive rates to predict mating competition among individuals qualified to mate. Behav. Ecol. 12, 397-401. (doi:10.1093/beheco/ 12.4.397)
13. Gerlach NM, McGlothlin JW, Parker PG, Ketterson ED. 2012 Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species. Behav. Ecol. 23, 1078-1088. (doi:10.1093/beheco/ars077)
14. Arnold SJ, Duvall D. 1994 Animal mating systems: a synthesis based on selection theory. Am. Nat. 143, 317-348. (doi:10.1086/285606)
15. Andersson M, Iwasa Y. 1996 Sexual selection. Trends Ecol. Evol. 11, 53-58. (doi:10.1016/01695347(96)81042-1)
16. Vincent A, Ahnesjö I, Berglund A, Rosenqvist G. 1992 Pipefishes and seahorses: are they all sex role reversed?. Trends Ecol. Evol. 7, 237-241. (doi:10. 1016/0169-5347(92)90052-D)
17. Snyder BF, Gowaty PA. 2007 A reappraisal of Bateman's classic study of intrasexual selection. Evolution 61, 2457-2468. (doi:10.1111/j.15585646.2007.00212.x)
18. Jones AG, Rosenqvist G, Berglund A, Arnold SJ, Avise JC. 2000 The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proc. R. Soc. Lond. B 267, 677-680. (doi:10.1098/ rspb.2000.1055)
19. Rodríguez-Muñoz R, Breitman A, Slate J, Walling CA, Tregenza T. 2010 Natural and sexual selection in a wild insect population. Science 328, 1269-1272. (doi:10.1126/science.1188102)
20. Jennions MD, Petrie M. 2000 Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21-64. (doi:10.1017/S0006323199005423)
21. Lehtonen J, Jennions MD, Kokko H. 2012 The many costs of sex. Trends Ecol. Evol. 27, 172-178. (doi:10.1016/j.tree.2011.09.016)
22. Magnhagen C. 1991 Predation risk as a cost of reproduction. Trends Ecol. Evol. 6, 183-186. (doi:10.1016/0169-5347(91)90210-O)
23. Jennions MD, Petrie M. 1997 Variation in mate choice and mating preferences: a review of causes and consequences. Biol. Rev. 72, 283-327. (doi:10.1017/S0006323196005014)
24. Altizer S et al. 2003 Social organization and parasite risk in mammals: Integrating theory and empirical studies. Ann. Rev. Ecol. Evol. Syst. 34, 517-547. (doi:10.1146/annurev.ecolsys.34.030102.151725)
25. Innocenti P, Morrow EH. 2009 Immunogenic males: a genome-wide analysis of reproduction and the cost of mating in Drosophila melanogaster females. J. Evol. Biol. 22, 964-973. (doi:10.1111/j.14209101.2009.01708.x)
26. Emlen ST, Wrege PH, Webster MS. 1998 Cuckoldry as a cost of polyandry in the sex-role-reversed wattled jacana, Jacana jacana. Proc. R. Soc. Lond. B 265, 2359-2364. (doi:10.1098/rspb.1998.0584)
27. Butchart SHM. 1999 Sexual conflicts and copulation patterns in polyandrous bronze-winged jacanas (Metopidius indicus). Behaviour 136, 443-468. (doi:10.1163/156853999501414)
28. Berglund A, Rosenqvist G. 2003 Sex role reversal in pipefish. Adv. Study Behav. 32, 131-167. (doi:10.1016/S0065-3454(03)01003-9)
29. McCoy EE, Jones AG, Avise JC. 2001 The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilise eggs and brood offspring externally. Mol. Ecol. 10, 1793-1800. (doi:10.1046/j.0962-1083.2001.01320.x)
30. Gwynne DT. 1984 Courtship feeding increases female reproductive success in bush crickets. Nature 307, 361-363. (doi:10.1038/307361a0)
31. Arnqvist G, Nilsson T. 2000 The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60, 145-164. (doi:10.1006/ anbe.2000.1446)
32. Simmons LW. 2005 The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Ann. Rev. Ecol. Evol. Syst. 36, 125-146. (doi:10.1146/annurev.ecolsys.36.102403.112501)
33. Wetton JH, Parkin DT. 1991 An association between fertility and cuckoldry in the house sparrow, Passer domesticus. Proc. R. Soc. Lond. B 245, 227-233. (doi:10.1098/rspb.1991.0114)
34. Garcia-Gonzalez F. 2004 Infertile matings and sperm competition: the effect of 'nonsperm representation' on intraspecific variation in sperm precedence patterns. Am. Nat. 164, 457-472. (doi:10.1086/ 423987)
35. Hasson O, Stone L. 2009 Male infertility, female infertility and extrapair copulations. Biol. Rev. 84, 225-244. (doi:10.1111/j.1469-185X.2008.00068.x)
36. Levitan DR. 1998 Sperm limitation, gamete competition, and sexual selection in external fertilizers. In Sperm competition and sexual selection (eds TR Birkhead, AP Møller), pp. 175-217. New York, NY: Academic Press.
37. Preston BT, Stevenson IR, Pemberton JM, Wilson K. 2001 Dominant rams lose out by sperm depletion. Nature 409, 681-682. (doi:10.1038/35055617)
38. Parker GA, Pizzari T. 2010 Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934.
39. Slatyer RA, Mautz BS, Backwell PRY, Jennions MD. 2012 Estimating genetic benefits of polyandry from experimental studies: a meta-analysis. Biol. Rev. 87, 1-33.(doi:10.1111/j.1469-185X.2011.00182.x)
40. Andersson M. 1994 Sexual selection. Princeton, NJ: Princeton University Press.
41. Zeh JA, Zeh DW. 1996 The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B 263, 1711-1717. (doi:10.1098/rspb.1996.0250)
42. Tregenza T, Wedell N. 2000 Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol. 9, 1013-1027. (doi:10.1046/j. 1365-294x.2000.00964.x)
43. Puurtinen M, Ketola T, Kotiaho JS. 2009 The good-genes and compatible-genes benefits of mate choice. Am. Nat. 174, 741-752. (doi:10.1086/606024)
44. Zeh JA, Zeh DW. 2001 Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61, 1051-1063. (doi:10.1006/anbe.2000.1705)
45. Roberts SC, Gosling LM. 2003 Genetic similarity and quality interact in mate choice decisions by female mice. Nat. Genet. 33, 103-106. (doi:10.1038/ ng1231)
46. Mays HL, Hill GE. 2004 Choosing mates: good genes versus genes that are a good fit. Trends Ecol. Evol. 19, 554-559. (doi:10.1016/j.tree.2004.07.018)
47. Zeh JA, Zeh DW. 1997 The evolution of polyandry. II. Post-copulatory defenses against genetic incompatibility. Proc. R. Soc. Lond. B 264, 69-75. (doi:10.1098/rspb.1997.0010)
48. Edward DA, Chapman T. 2011 The evolution and significance of male mate choice. Trends Ecol. Evol. 26, 647-654. (doi:10.1016/j.tree.2011.07.012)
49. Colegrave N, Kotiaho JS, Tomkins JL. 2002 Mate choice or polyandry: reconciling genetic compatibility and good genes sexual selection. Evol. Ecol. Res. 4, 911-917.
50. Price TAR, Hodgson DJ, Lewis Z, Hurst GDD, Wedell N. 2008 Selfish genetic elements promote polyandry in a fly. Science 322, 1241-1243. (doi:10.1126/ science.1163766)
51. Champion de Crespigny FE, Hurst LD, Wedell N. 2008 Do Wolbachia-associated incompatibilities promote polyandry? Evolution 62, 107-122. (doi:10.1111/j.1558-5646.2007.00274.x)
52. Michalczyk L, Millard AL, Martin OY, Lumley AJ, Emerson BC, Chapman T, Gage MJG. 2011 Inbreeding promotes female promiscuity. Science 333, 1739-1742. (doi:10.1126/science.1207314)
53. Keller L, Reeve HK. 1995 Why do females mate with multiple males: the sexually selected sperm hypothesis. Adv. Study Behav. 24, 291-315. (doi:10.1016/S0065-3454(08)60397-6)
54. Pizzari T, Birkhead TR. 2002 The sexually-selected sperm hypothesis: sex biased inheritance and sexual antagonism. Biol. Rev. 77, 183-209. (doi:10.1017/ S1464793101005863)
55. Yasui Y. 1997 A 'good-sperm' model can explain the evolution of costly multiple mating by females. Am. Nat. 149, 573-584. (doi:10.1086/286006)
56. Evans JP, Simmons LW. 2008 The genetic basis of traits regulating sperm competition and polyandry: can selection favour the evolution of good-and sexy-sperm? Genetica 134, 5-19. (doi:10.1007/ s10709-007-9162-5)
57. Firman RC, Simmons LW. 2012 Male house mice evolving with post-copulatory sexual selection sire embryos with increased viability. Ecol. Lett. 15, 42-46. (doi:10.1111/j.1461-0248. 2011.01706.x)
58. Stockley P. 2003 Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc. R. Soc. Lond. B 270, 271-278. (doi:10.1098/rspb.2002.2228)
59. Yasui Y. 1998 The 'genetic benefits' of female multiple mating reconsidered. Trends Ecol. Evol. 13, 246-250. (doi:10.1016/S0169-5347(98)01383-4)
60. Crean AJ, Marshall DJ. 2009 Coping with environmental uncertainty: dynamic bet hedging as a maternal effect. Phil. Trans. R. Soc. B 364, 1087-1096. (doi:10.1098/rstb.2008.0237)
61. Aguirre JD, Marshall DJ. 2012 Does genetic diversity reduce sibling competition? Evolution 66, 94-102. (doi:10.1111/j.1558-5646.2011.01413.x)
62. Forsman A, Ahnesjö J, Caesar S. 2007 Fitness benefits of diverse offspring in pygmy grasshoppers. Evol. Ecol. Res. 9, 1305-1318.
63. Baer B, Schmid-Hempel P. 1999 Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151-154. (doi:10.1038/16451)
64. Sagebakken G, Ahnesjö I, Braga Goncalves I, Kvarnemo C. 2011 Multiply-mated males show higher embryo survival in a paternally caring fish. Behav. Ecol. 22, 625-629. (doi:10.1093/beheco/ arr023)
65. McLeod L, Marshall DJ. 2009 Do genetic diversity effects drive the benefits associated with multiple mating? A test in a marine invertebrate. PLoS ONE 4, e6347. (doi:10.1371/journal.pone.0006347)
66. Gowaty PA, Hubbell SP. 2005 Chance, time allocation, and the evolution of adaptively flexible sex role behaviour. Integr. Comp. Behav. 45, 931-944. (doi:10.1093/icb/45.5.931)
67. Simmons LW. 1990 Nuptial feeding in tettigoniids: male costs and the rates of fecundity increase. Behav. Ecol. Sociobiol. 27, 43-47.
68. Simmons LW, Gwynne DT. 1993 Reproductive investment in bush crickets: the allocation of male and female nutrients to offspring. Proc. R. Soc. Lond. B 252, 1-5. (doi:10.1098/rspb.1993.0038)
69. Simmons LW, Gwynne DT. 1991 The refractory period of female katydids (Orthoptera: Tettigoniidae): sexual conflict over the remating interval?. Behav. Ecol. 2, 276-282.
70. Simmons LW. 1995 Relative parental expenditure, potential reproductive rates, and the control of sexual selection in katydids. Am. Nat. 145, 797-808. (doi:10.1086/285768)
71. Gwynne DT, Simmons LW. 1990 Experimental reversal of courtship roles in an insect. Nature 346, 172-174. (doi:10.1038/346172a0)
72. Simmons LW, Bailey WJ. 1990 Resource influenced sex roles of zaprochiline tettigoniids (Orthoptera: Tettigoniidae). Evolution 44, 1853-1868. (doi:10. 2307/2409513)
73. Gwynne DT, Bailey WJ. 1999 Female - female competition in katydids: sexual selection for increased sensitivity to a male signal? Evolution 53, 546-551. (doi:10.2307/2640790)
74. Bailey WJ, Romer H. 1991 Sexual differences in auditory sensitivity: mismatch of hearing threshold and call frequency in a tettigoniid (Orthotera, Tettigoniidae: Zaprochilinae). J. Comp. Phys. A 169, 349-353.
75. Bailey WJ, Simmons LW. 1991 Male-male behavior and sexual dimorphism of the ear of a zaprochiline tettigoniid (Orthoptera: Tettigoniidae). J. Insect Behav. 4, 51-65. (doi:10.1007/BF01092551)
76. Forsgren E, Amundsen T, Borg ÅA, Bjelvenmark J. 2004 Unusually dynamic sex roles in a fish. Nature 429, 551-554. (doi:10.1038/nature02562)
77. Rosvall KA. 2011 Intrasexual competition in females: evidence for sexual selection?. Behav. Ecol. 22, 1131-1140. (doi:10.1093/beheco/arr106)
78. Stockley P, Bro-Jørgensen J. 2011 Female competition and its evolutionary consequences in mammals. Biol. Rev. 86, 341-366. (doi:10.1111/j. 1469-185X.2010.00149.x)
79. Karvonen E, Rintamäki PT, Alatalo RV. 2000 Female-female aggression and female mate choice on black grouse leks. Anim. Behav. 59, 981-987. (doi:10.1006/anbe.1999.1379)
80. Petrie M, Hall M, Halliday T, Budgey H, Pierpoint C. 1992 Multiple mating in a lekking bird: why do peahens mate with more than one male and with the same male more than once?. Behav. Ecol. Sociobiol. 31, 349-358.
81. Warner RR, Shapiro DY, Marconato A, Petersen CW. 1995 Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females. Proc. R. Soc. Lond. B 262, 135-139. (doi:10.1098/rspb.1995.0187)
82. Jones TM. 2001 A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis. J. Insect Behav. 14, 385-399. (doi:10.1023/A:101112 7514317)
83. Clutton-Brock TH. 2009 Sexual selection in females. Anim. Behav. 77, 3-11. (doi:10.1016/j.anbehav. 2008.08.026)
84. Heinsohn R, Legge S, Endler JA. 2005 Extreme reversed sexual dichromatism in a bird without sex role reversal. Science 309, 617-619. (doi:10.1126/ science.1112774)
85. Amundsen T. 2000 Why are female birds ornamented?. Trends Ecol. Evol. 15, 149-155. (doi:10.1016/S0169-5347(99)01800-5)
86. Watson NL, Simmons LW. 2010 Reproductive competition promotes the evolution of female weaponry. Proc. R. Soc. B 277, 2035-2040. (doi:10. 1098/rspb.2009.2335)
87. Heubel KU, Lindström K, Kokko H. 2008 Females increase current reproductive effort when future access to males is uncertain. Biol. Lett. 4, 224-227. (doi:10.1098/rsbl.2007.0630)
88. Berglund A. 1991 Egg competition in a sex-role reversed pipefish: subdominant females trade reproduction for growth. Evolution 45, 770-774. (doi:10.2307/2409928)
89. 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. Proc. R. Soc. Lond. B 270, 633-640. (doi:10.1098/rspb.2002.2268)
90. Clutton-Brock T. 1989 Mammalian mating systems. Proc. R. Soc. Lond. B 236, 339-372. (doi:10.1098/rspb.1989.0027)
91. Pomfret JC, Knell RJ. 2008 Crowding, sex ratio and horn evolution in a South African beetle community. Proc. R. Soc. B 275, 315-321. (doi:10.1098/rspb.2007.1498)
92. Deinert EL. 2003 Mate location and competition for mates in a pupal mating butterfly. In Butterflies: ecology and evolution taking flight (eds CL Boggs, WB Watt, PR Ehrlich), pp. 91-108. Chicago, IL: University of Chicago Press.
93. Paxton RJ. 2005 Male mating behaviour and mating systems of bees: an overview. Apidologie 36, 145-156. (doi:10.1051/apido:2005007)
94. Wiklund C, Forsberg J. 1991 Sexual size dimorphism 13 in relation to female polygamy and protandry in butterflies: a comparative study of Swedish Pieridae and Satyridae. Oikos 60, 373-381. (doi:10.2307/ 3545080)
95. Simmons LW, Llorens T, Schinzig M, Hosken D, Craig M. 1994 Sperm competition selects for male mate choice and protandry in the bushcricket, Requena verticalis (Orthoptera: Tettigoniidae). Anim. Behav. 47, 117-122. (doi:10.1006/anbe.1994.1013)
96. Parker GA. 1970 Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525-567. (doi:10.1111/j.1469-185X.1970.tb01176.x)
97. Simmons LW. 2001 Sperm competition and its evolutionary consequences in the insects. Princeton, NJ: Princeton University Press.
98. Eberhard WG. 1996 Female control: sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.
99. Partridge C, Ahnesjö I, Kvarnemo C, Mobley KB, Berglund A, Jones AG. 2009 The effect of perceived female parasite load on post-copulatory male choice in a sex-role-reversed pipefish. Behav. Ecol. Sociobiol. 63, 345-354. (doi:10.1007/s00265-0080668-3)
100. Birkhead TR, Møller AP. 1998 Sperm competition and sexual selection. New York, NY: Academic Press
101. Birkhead TR, Møller AP. 1992 Sperm competition in birds: evolutionary causes and consequences. New York, NY: Academic Press.
102. Waage JK. 1979 Dual function of the damselfly penis: sperm removal and transfer. Science 203, 916-918. (doi:10.1126/science.203.4383.916)
103. Córdoba-Aguilar A. 1999 Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly. Proc. R. Soc. Lond. B 266, 779-784. (doi:10.1098/rspb.1999.0705)
104. Córdoba-Aguilar A. 2002 Sensory trap as the mechanism of sexual selection in a damselfly genitalic trait (Insecta: Calopterygidae). Am. Nat. 160, 594-601. (doi:10.1086/342819)
105. Arnqvist G. 1998 Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784-786. (doi:10.1038/31689)
106. Simmons LW, Garcia-Gonzalez F. 2011 Experimental coevolution of male and female genital morphology. Nat. Commun. 2, 374. (doi:10.1038/ ncomms1379)
107. Perry JC, Rowe L. 2012 Sexual conflict and antagonistic coevolution across water strider populations. Evolution 66, 544-557. (doi:10.1111/j. 1558-5646.2011.01464.x)
108. Evans JP, Gasparini C, Holwell GI, Ramnarine IW, Pitcher TE, Pilastro A. 2011 Intraspecific evidence from guppies for correlated patterns of male and female genital trait diversification. Proc. R. Soc. B 278, 2611-2620. (doi:10.1098/rspb.2010.2453)
109. Siva-Jothy MT. 1987 Variation in copulation duration and the resultant degree of sperm removal in Orthetrum cancellatum (L.) (Libellulidae: Odonata). Behav. Ecol. Sociobiol. 20, 147-151. (doi:10.1111/j. 1558-5646.2012.01741.x)
110. Parker GA. 1970 Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. J. Insect Phys. 16, 1301-1328. (doi:10.1016/0022-1910(70)90131-9)
111. Simmons LW, Parker GA, Stockley P. 1999 Sperm displacement in the yellow dung fly, Scatophaga stercoraria: an investigation of male and female processes. Am. Nat. 153, 302-314. (doi:10.1086/ 303171)
112. Møller AP, Birkhead TR. 1989 Copulation behavior in mammals: evidence that sperm competition is widespread. Biol. J. Linn. Soc. 38, 119-131. (doi:10.1111/j.1095-8312.1989.tb01569.x)
113. Devine MC. 1977 Copulatory plugs, restricted mating opportunities and reproductive competition among male garter snakes. Nature 267, 345-346. (doi:10.1038/267345a0)
114. Shine R, Olsson MM, Mason RT. 2000 Chastity belts in gartersnakes: the functional significance of mating plugs. Biol. J. Linn. Soc. 70, 377-390. (doi:10.1111/j.1095-8312.2000.tb01229.x)
115. Ramm SA, Parker GA, Stockley P. 2005 Sperm competition and the evolution of male reproductive anatomy in rodents. Proc. R. Soc. B 272, 949-955. (doi:10.1098/rspb.2004.3048)
116. Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD. 2008 Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Mol. Biol. Evol. 25, 207-219. (doi:10.1093/molbev/ msm242)
117. Ramm SA, McDonald L, Hurst JL, Beynon RJ, Stockley P. 2009 Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Mol. Biol. Evol. 26, 189-198. (doi:10.1093/molbev/msn237)
118. Dean MD, Findlay GD, Hoopman MR, Wu CC, MacCoss MJ, Swanson WJ, Nachman MW. 2011 Identification of ejaculated proteins in the house mouse (Mus domesticus) via isotopic labeling. BMC Genomics 12, 306. (doi:10.1186/1471-2164-12-306)
119. Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT. 2004 Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nat. Genet. 36, 1326-1329. (doi:10. 1038/ng1471)
120. Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF. 2011 Insect seminal fluid proteins: identification and function. Ann. Rev. Entomol. 56, 21-40. (doi:10.1146/annurev-ento-120709-144823)
121. Haerty W et al. 2007 Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177, 1321-1335. (doi:10.1534/genetics. 107.078865)
122. Wagstaff BJ, Begun DJ. 2007 Adaptive evolution of recently duplicated accessory gland protein genes in desert drosophila. Genetics 177, 1023-1030. (doi:10.1534/genetics.107.077503)
123. Vahed K, Gilbert FS. 1996 Differences across taxa in nuptial gift size correlate with differences in sperm number and ejaculate volume in bushcrickets (Orthoptera: Tettigoniidae). Proc. R. Soc. Lond. B 263, 1257-1265. (doi:10.1098/rspb.1996.0185)
124. Estrada C, Schulz S, Yildizhan S, Gilbert LE. 2011 Sexual selection drives the evolution of antiaphrodisiac pheromones in butterflies. Evolution 65, 2843-2854. (doi:10.1111/j.1558-5646.2011. 01352.x)
125. Dickinson JL. 1995 Trade-offs between post-copulatory riding and mate location in the blue milkweed beetle. Behav. Ecol. 6, 280-286. (doi:10. 1093/beheco/6.3.280)
126. Vahed K. 2007 Comparative evidence for a cost to males of manipulating females in bushcrickets. Behav. Ecol. 18, 499-506. (doi:10.1093/beheco/ arm021)
127. Schubert M, Schradin C, Rödel HG, Pillay N, Ribble DO. 2009 Male mate guarding in a socially monogamous mammal, the round-eared sengi: on costs and trade-offs. Behav. Ecol. Sociobiol. 64, 257-264. (doi:10.1007/s00265-009-0842-2)
128. Komdeur J. 2001 Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proc. R. Soc. Lond. B 268, 2103-2111. (doi:10.1098/rspb.2001.1750)
129. Cuadrado M. 2000 Influence of female's sexual stage and number of available males on the intensity of guarding behavior by male common chameleons: a test of different predictions. Herpetologica 56, 387-393.
130. McMillan VE. 1991 Variable mate guarding behavior in the dragonfly Plathemis lydia (Odonata: Libellulidae). Anim. Behav. 41, 979-988. (doi:10.1016/S0003-3472(05)80636-0)
131. Vepsäläinen K, Savolainen R. 1995 Operational sex ratios and mating conflict between the sexes in the water strider Gerris lacustris. Am. Nat. 146, 869-880. (doi:10.1086/285829)
132. McLain DK. 1980 Female choice and the adaptive significance of prolonged copulation in Nezara viridula (Hemiptera: Pentatomaidae). Psyche 87, 325-336. (doi:10.1155/1980/70498)
133. Hunt J, Simmons LW. 2002 Confidence of paternity and paternal care: covariation revealed through the experimental manipulation of the mating system in the beetle Onthophagus taurus. J. Evol. Biol. 15, 784-795. (doi:10.1046/j.1420-9101.2002.00442.x)
134. Bretman A, Fricke C, Chapman T. 2009 Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc. R. Soc. B 276, 1705-1711. (doi:10.1098/rspb.2008.1878)
135. Sirot LK, Wolfner MF, Wigby S. 2011 Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 108, 9922-9926. (doi:10. 1073/pnas.1100905108)
136. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, Wolfner MF, Chapman T. 2009 Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19, 751-757. (doi:10.1016/j.cub.2009.03.036)
137. Dewsbury DA. 1982 Ejaculate cost and male choice. Am. Nat. 119, 601-610. (doi:10.1086/283938)
138. Hayward A, Gillooly JF. 2011 The cost of sex: quantifying energetic investment in gamete production by males and females. PLoS ONE 6, 14 e16557. (doi:10.1371/journal.pone.0016557)
139. Sirot LK, Buehner N, Fiumera AC, Wolfner MF. 2009 Seminal fluid protein depletion and replenishment in the fruit fly, Drosophila melanogaster: an ELISA-based method for tracking individual ejaculates. Behav. Ecol. Sociobiol. 63, 1505-1513. (doi:10.1007/s00265-009-0806-6)
140. Doyle JM. 2011 Sperm depletion and a test of the phenotype-linked fertility hypothesis in gray treefrogs (Hyla versicolor). Can. J. Zool. 89, 853-858. (doi:10.1139/z11-060)
141. Olsson M, Madsen T, Shine R. 1997 Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264, 455-459. (doi:10.1098/rspb.1997.0065)
142. Birkhead TR, Fletcher F. 1995 Depletion determines sperm numbers in male zebra finches. Anim. Behav. 49, 451-456. (doi:10.1006/anbe. 1995.0058)
143. Poulin R, Morand S. 2000 Testes size, body size and male-male competition in acanthocephalan parasites. J. Zool. 250, 551-558.
144. Fry CL. 2006 Juvenile hormone mediates a trade-off between primary and secondary sexual traits in stalk-eyed flies. Evol. Dev. 8, 191-201. (doi:10. 1111/j.1525-142X.2006.00089.x)
145. Simmons LW, Emlen DJ. 2006 Evolutionary trade-off between weapons and testes. Proc. Natl Acad. Sci. USA 103, 16 349-16 351.
146. Yamane T, Okada K, Nakayama S, Miyatake T. 2010 Dispersal and ejaculatory strategies associated with exaggeration of weapon in an armed beetle. Proc. R. Soc. B 277, 1705-1710. (doi:10.1098/rspb. 2009.2017)
147. Simmons LW, Tinghitella RM, Zuk M. 2010 Quantitative genetic variation in courtship song and its covariation with immune function and sperm quality in the field cricket Teleogryllus oceanicus. Behav. Ecol. 21, 1330-1336. (doi:10.1093/beheco/ arq154)
148. Montrose VT, Harris WE, Moore AJ, Moore PJ. 2008 Sperm competition within a dominance hierarchy: investment in social status versus investment in ejaculates. J. Evol. Biol. 21, 1290-1296. (doi:10.1111/j.1420-9101.2008.01570.x)
149. Engqvist L. 2011 Male attractiveness is negatively genetically associated with investment in copulations. Behav. Ecol. 22, 345-349. (doi:10.1093/beheco/arq211)
150. Demary KC, Lewis SM. 2007 Male courtship attractiveness and paternity success in Photinus greeni fireflies. Evolution 61, 431-439. (doi:10. 1111/j.1558-5646.2007.00033.x)
151. Kelly CD. 2008 Sperm investment in relation to weapon size in a male trimorphic insect? Behav. Ecol. 19, 1018-1024.
152. Parker GA, Lessells CM, Simmons LW. In press. Sperm competition games: a general model for precopulatory male-male competition. Evolution. (doi:10.1111/j.1558-5646.2012.01741.x)
153. Pitcher TE, Doucet SM, Beausoleil J-MJ, Hanley D. 2009 Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. J. Fish Biol. 74, 1450-1461. (doi:10.1111/j.1095-8649.2009. 02210.x)
154. Liljedal S, Folstad I, Skarstein F. 1999 Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proc. R. Soc. Lond. B 266, 1893-1898. (doi:10.1098/rspb.1999.0863)
155. Rudolfsen G, Figenschou L, Folstad I, Tveiten H, Figenschou M. 2006 Rapid adjustments of sperm characteristics in relation to social status. Proc. R. Soc. B 273, 325-332. (doi:10.1098/rspb.2005.3305)
156. Evans JP. 2010 Quantitative genetic evidence that males trade attractiveness for ejaculate quality in guppies. Proc. R. Soc. B 277, 3195-3202. (doi:10. 1098/rspb.2010.0826)
157. Kvarnemo C, Manson W, Svensson O. 2010 Investment in testes, sperm-duct glands and lipid reserves differs between male morphs but not between early and late breeding season in Pomatoschistus minutus. J. Fish Biol. 76, 1609-1625. (doi:10.1111/j.1095-8649.2010.02587.x)
158. Preston BT, Jalme MS, Hingrat Y, Lacroix F, Sorci G. 2011 Sexually extravagant males age more rapidly. Ecol. Lett. 14, 1017-1024. (doi:10.1111/j.14610248.2011.01668.x)
159. Pizzari T, Cornwallis CK, Froman DP. 2007 Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proc. R. Soc. B 274, 853-860. (doi:10.1098/rspb.2006.0080)
160. Rowe M, Swaddle JP, Pruett-Jones S, Webster MS. 2010 Plumage coloration, ejaculate quality and reproductive phenotype in the red-backed fairy-wren. Anim. Behav. 79, 1239-1246. (doi:10.1016/j. anbehav.2010.02.020)
161. Fitzpatrick JL, Almbro M, Gonzalez-Voyer A, Kolm N, Simmons LW. 2012 Male contest competition and the coevolution of weaponry and testes in pinnipeds. Evolution 66, 3595-3604. (doi:10.1111/ j.1558-5646.2012.01713.x)
162. Simmons LW, Peters M, Rhodes G. 2011 Low pitched voices are perceived as masculine and attractive but do they predict semen quality in men? PLoS ONE 6, e29271. (doi:10.1371/journal. pone.0029271)
163. Kokko H, Rankin DJ. 2006 Lonely hearts or sex in the city? Density-dependent effects in mating systems. Phil. Trans. R. Soc. B 361, 319-334. (doi:10.1098/rstb.2005.1784)
164. Simmons LW, Fitzpatrick JL. 2012 Sperm wars and the evolution of male fertility. Reproduction 144, 519-534. (doi:10.1530/REP-12-0285)
165. Hosken DJ, Ward PI. 2001 Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4, 10-13. (doi:10.1046/j.1461-0248.2001. 00198.x)
166. Simmons LW, García-González F. 2008 Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution 62, 2580-2591. (doi:10.1111/j.1558-5646.2008.00479.x)
167. Firman RC, Simmons LW. 2010 Experimental evolution of sperm quality via postcopulatory sexual selection in house mice. Evolution 64, 1245-1256.
168. Firman RC, Simmons LW. 2010 Experimental evolutin of sperm competitiveness in a mammal. BMC Evol. Biol. 11, 19.
169. Firman RC, Simmons LW. 2008 The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J. Evol. Biol. 21, 1524-1533. (doi:10.1111/j.1420-9101. 2008.01612.x)
170. Dziminski MA, Roberts JD, Beveridge M, Simmons LW. 2010 Among-population covariation between sperm competition and ejaculate expenditure in frogs. Behav. Ecol. 21, 322-328. (doi:10.1093/ beheco/arp191)
171. Brown CR, Brown MB. 2003 Testis size increases with colony size in cliff swallows. Behav. Ecol. 14, 569-575. (doi:10.1093/beheco/arg030)
172. Ramm SA, Stockley P. 2009 Adaptive plasticity of mammalian sperm production in response to social experience. Proc. R. Soc. B 276, 745-751. (doi:10. 1098/rspb.2008.1296)
173. delBarco-Trillo J, Ferkin MH. 2004 Male mammals respond to a risk of sperm competition conveyed by odours of conspecific males. Nature 431, 446-449. (doi:10.1038/nature02845)
174. Pilastro A, Scaggiante M, Rasotto MB. 2002 Individual adjustement of sperm expenditure accords with sperm competition theory. Proc. Natl Acad. Sci. USA 99, 9913-9915. (doi:10.1073/pnas.152133499)
175. Smith CC, Ryan MJ. 2011 Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis. Biol. Lett. 7, 733-735. (doi:10.1098/rsbl. 2011.0286)
176. Pizzari T, Cornwallis CK, Løvlie H, Jakobsson S, Birkhead TR. 2003 Sophisticated sperm allocation in male fowl. Nature 426, 70-74. (doi:10.1038/ nature02004)
177. Gage MJG. 1991 Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit fly. Anim. Behav. 42, 1036-1037. (doi:10.1016/S00033472(05)80162-9)
178. Kelly CD, Jennions MD. 2011 Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol. Rev. 86, 863-884. (doi:10.1111/j. 1469-185X.2011.00175.x)
179. delBarco-Trillo J. 2011 Adjustment of sperm allocation under high risk of sperm competition across taxa: a meta-analysis. J. Evol. Biol. 24, 1706-1714. (doi:10.1111/j.1420-9101.2011.02293.x)
180. Engqvist L, Reinhold K. 2005 Pitfalls in experiments testing predictions from sperm competition theory. J. Evol. Biol. 18, 116-123. (doi:10.1111/j.14209101.2004.00792.x)
181. Thomas ML, Simmons LW. 2008 Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets. Proc. R. Soc. B 276, 383-388. (doi:10.1098/rspb. 2008.1206)
182. Gage AR, Barnard CJ. 1996 Male crickets increase sperm number in relation to competition and female size. Behav. Ecol. Sociobiol. 38, 349-353. (doi:10.1007/s002650050251)
183. Cornwallis CK, Birkhead TR. 2007 Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity. 15 Proc. R. Soc. B 274, 583-590. (doi:10.1098/rspb. 2006.3757)
184. Simmons LW, Parker GA. 1996 Parental investment and the control of sexual selection: can sperm competition affect the direction of sexual competition? Proc. R. Soc. Lond. B 263, 515-519. (doi:10.1098/rspb.1996.0078)
185. Lorch PD. 2002 Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition? Am. Nat. 159, 645-657. (doi:10.1086/339992)
186. Parker GA, Ball MA, Stockley P, Gage MJG. 1996 Sperm competition games: individual assessment of sperm competition intensity by group spawners. Proc. R. Soc. Lond. B 263, 1291-1297. (doi:10.1098/rspb.1996.0189)
187. Simmons LW. 1995 Courtship feeding in katydids (Orthoptera: Tettigoniidae): investment in offspring and in obtaining fertilizations. Am. Nat. 146, 307-315. (doi:10.1086/285801)
188. Gwynne DT. 1986 Courtship feeding in katydids (Orthoptera: Tettigoniidae): investment in offspring or in obtaining fertilizations? Am. Nat. 128, 342-352. (doi:10.1086/284566)
189. Simmons LW. 1992 Quantification of role reversal in relative parental investment in a bushcricket. Nature 358, 61-63. (doi:10.1038/358061a0)
190. Queller DC. 1997 Why do females care more than males? Proc. R. Soc. Lond. B 264, 1555-1557. (doi:10.1098/rspb.1997.0216)
191. Whittingham LA, Taylor PD, Robertson RJ. 1992 Confidence of paternity and male parental care. Am. Nat. 139, 1115-1125. (doi:10.1086/285376)
192. Xia X. 1992 Uncertainty of paternity can select against paternal care. Am. Nat. 139, 1126-1129. (doi:10.1086/285377)
193. Wright J. 1998 Paternity and paternal care. In Sperm competition and sexual selection (eds TR Birkhead, AP Møller), pp. 117-145. New York, NY: Academic Press.
194. Alonzo SH. 2009 Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol. Evol. 25, 99-108. (doi:10.1016/j.tree.2009.07.012)
195. Kokko H, Jennions MD. 2008 Parental investment, sexual selection and sex ratios. J. Evol. Biol. 21, 919-948. (doi:10.1111/j.1420-9101.2008.01540.x)
196. Møller AP. 2000 Male parental care, female reproductive success and extra-pair paternity. Behav. Ecol. 11, 161-168. (doi:10.1093/beheco/11.2.161)
197. Griffith SC, Owens IPF, Thuman KA. 2002 Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195-2212. (doi:10.1046/j.1365-294X.2002.01613.x)
198. Møller AP. 1988 Female choice selects for male sexual tail ornaments in the monogamous swallow. Nature 332, 640-642. (doi:10.1038/332640a0)
199. 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. (doi:10.1126/science.250.4986.1394)
200. Sheldon BC, Ellegren H. 1999 Sexual selection resulting from extrapair paternity in collared flycatchers. Anim. Behav. 57, 285-298. (doi:10. 1006/anbe.1998.0968)
201. Møller AP, Birkhead TR. 1994 The evolution of plumage brightness in birds is related to extrapair paternity. Evolution 48, 1089-1100. (doi:10.2307/ 2410369)
202. Møller AP. 1998 Sperm competition and sexual selection. In Sperm competition and sexual selection (eds TR Birkhead, AP Møller), pp. 55-90. New York, NY: Academic Press.
203. Kvarnemo C. 1994 Temperature differentially affects male and female reproductive rates in the sand goby: consequences for operational sex ratio. Proc. R. Soc. Lond. B 256, 151-156. (doi:10.1098/ rspb.1994.0063)
204. Jones AG, Walker D, Kvarnemo C, Lindström K, Avise JC. 2001 How cuckoldry can decrease the opportunity for sexual selection: data and theory from a genetic parentage analysis of the sand goby, Pomatoschistus minutus. Proc. Natl Acad. Sci. USA 98, 9151-9156. (doi:10.1073/pnas.171310198)
205. Hunt J, Breuker CJ, Sadowski JA, Moore AJ. 2009 Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22, 13-26. (doi:10.1111/j.1420-9101. 2008.01633.x)
206. Parker GA. 2006 Sexual conflict over mating and fertilization: an overview. Phil. Trans. R. Soc. B 361, 235-259. (doi:10.1098/rstb.2005.1785)
207. Forsgren E. 1997 Female sand gobies prefer good fathers over dominant males. Proc. R. Soc. Lond. B 264, 1283-1286. (doi:10.1098/rspb.1997.0177)
208. Pemberton JM, Coltman DW, Smith JA, Pilkington JG. 1999 Molecular analysis of a promiscuous, fluctuating mating system. Biol. J. Linn. Soc. 68, 289-301. (doi:10.1111/j.1095-8312.1999.tb01170.x)
209. Danielsson I. 2000 Antagonistic pre-and post-copulatory sexual selection on male body size in a water strider (Gerris lacustris). Proc. R. Soc. Lond. B 268, 77-81. (doi:10.1098/rspb.2000.1332)
210. Endler JA. 1988 Sexual selection and predation risk in guppies. Nature 332, 593-594. (doi:10.1038/ 332593b0)
211. Houde AE. 1997 Sex, color and mate choice in guppies. Princeton, NJ: Princeton University Press.
212. Pilastro A, Simonata M, Bisazza A, Evans JP. 2004 Cryptic female preference for colorful males in guppies. Evolution 58, 665-669.
213. Evans JP, Zane L, Francescato S, Pilastro A. 2003 Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421, 360-363. (doi:10.1038/nature01367)
214. Roff DA. 2002 Life history evolution. Sunderland, MA: Sinauer Associates.
215. van Noordwijk AJ, de Jong G. 1986 Acquisition and allocation of resources: their influence on variation in life history tactics. Am. Nat. 128, 137-142. (doi:10.1086/284547)
216. Reznick D, Nunney L, Tessier A. 2000 Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol. Evol. 15, 421-425. (doi:10.1016/ S0169-5347(00)01941-8)
217. Malo AF, Roldan ERS, Garde J, Soler AJ, Gomendio M. 2005 Antlers honestly advertise sperm production and quality. Proc. R. Soc. B 272, 149-157. (doi:10.1098/rspb.2004.2933)
218. Locatello L, Rasotto MB, Evans JP, Pilastro A. 2006 Colourful male guppies produce faster and more viable sperm. J. Evol. Biol. 19, 1595-1602. (doi:10.1111/j.1420-9101.2006.01117.x)
219. Rowe L, Houle D. 1996 The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415-1421. (doi:10.1098/rspb.1996.0207)
220. Wilkinson GS, Taper M. 1999 Evolution of genetic variation for condition-dependent traits in stalk-eyed flies. Proc. R. Soc. Lond. B 266, 1685-1690. (doi:10.1098/rspb.1999.0832)
221. Simmons LW, Kotiaho JS. 2002 Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56, 1622-1631.
222. Kotiaho JS, Simmons LW, Tomkins JL. 2001 Towards a resolution of the lek paradox. Nature 410, 684-686. (doi:10.1038/35070557)
223. Simmons LW, Kotiaho JS. 2007 Quantitative genetic correlation between trait and preference supports a sexually selected sperm process. Proc. Natl Acad. Sci. USA 104, 16 604-16 608. (doi:10.1073/pnas. 0704871104)
224. García-González F, Simmons LW. 2007 Shorter sperm confer higher competitive fertilization success. Evolution 61, 816-824. (doi:10.1111/j. 1558-5646.2007.00084.x)
225. García-González F, Simmons LW. 2011 Good genes and sexual selection in dung beetles (Onthophagus taurus): genetic variance in egg-to-adult and adult viability. PLoS ONE 6, e16233. (doi:10.1371/journal. pone.0016233)
226. Simmons LW, Holley R. 2011 Offspring viability benefits but no apparent costs of mating with high quality males. Biol. Lett. 7, 419-421. (doi:10.1098/ rsbl.2010.0976)
227. Pischedda A, Rice WR. 2012 Partitioning sexual selection into its mating success and fertilization success components. Proc. Natl Acad. Sci. USA 109, 16 2049-2053. (doi:10.1073/pnas.1110841109)
228. Birkhead TR, Atkin L, Møller AP. 1987 Copulation behaviour of birds. Behaviour 101, 101-138. (doi:10.1163/156853987X00396)
229. Alatalo RV, Burke T, Dann J, Hanotte O, Höglund J, Lundberg A, Moss R, Rintamäki PT. 1996 Paternity, copulation disturbance and female choice in lekking black grouse. Anim. Behav. 52, 861-873. (doi:10. 1006/anbe.1996.0234)
230. Kokko H, Sutherland WJ, Lindström J, Reynolds JD, Mackenzie A. 1998 Individual mating success, lek stability, and the neglected limitations of statistical power. Anim. Behav. 56, 755-762. (doi:10.1006/ anbe.1998.0815)
231. Hingrat Y, Saint Jalme M, Chalah T, Orhant N, Lacroix F. 2008 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. 39, 393-404. (doi:10.1111/j.0908-8857.2008.03994.x)
232. Lesobre L, Lacroix F, Le Nuz E, Hingrat Y, Chalah T, Jaime MS. 2010 Absence of male reproductive skew, along with high frequency of polyandry and conspecific brood parasitism in the lekking Houbara bustard Chlamydotis undulata undulata. J. Avian Biol. 41, 117-127. (doi:10.1111/j.1600-048X.2009. 04794.x)
233. Lanctot RB, Scribner KT, Kempenaers B, Weatherhead PJ. 1997 Lekking without a paradox in the buff-breasted sandpiper. Am. Nat. 149, 1051-1070. (doi:10.1086/286038)
234. Lank DB, Smith CM, Hanotte O, Ohtonen A, Bailey S, Burke T. 2002 High frequency of polyandry in a lek mating system. Behav. Ecol. 13, 209-215. (doi:10.1093/beheco/13.2.209)
235. Collet J, Richardson DS, Worley K, Pizzari T. 2012 Sexual selection and the differential effect of polyandry. Proc. Natl Acad. Sci. USA 109, 8641-8645. (doi:10.1073/pnas.1200219109)
236. Peters A, Denk AG, Delhey K, Kempenaers B. 2004 Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J. Evol. Biol. 17, 1111-1120. (doi:10.1111/j.1420-9101.2004.00743.x)
237. Helfenstein F, Losdat S, Møller AP, Blout JD, Richner H. 2010 Sperm of colourful males are better protected against oxidative stress. Ecol. Lett. 13, 213-222. (doi:10.1111/j.1461-0248. 2009.01419.x)
238. Pike TW, Blount JD, Lindström J, Metcalf NB. 2010 Dietary carotenoid availability, sexual signalling and functional fertility in sticklebacks. Biol. Lett. 6, 191-193. (doi:10.1098/rsbl.2009.0815)