How multiple mating by females affects sexual selection

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1613, 2013, Pages

  Shuster, Stephen M ^a   Briggs, William R ^a   Dennis, Patricia A ^a  

^a NORTHERN ARIZONA UNIVERSITY   (United States)

Author keywords

Cryptic female choice; Female life history; Opportunity for sexual selection; Polyandrous mating; Post mating sexual selection; Sperm competition

Indexed keywords

COVARIANCE ANALYSIS; DATA PROCESSING; FEMALE BEHAVIOR; FITNESS; MATING BEHAVIOR; POLYANDRY; REPRODUCTION; SEXUAL SELECTION; SPERM COMPETITION;

ANIMAL; BIOLOGICAL MODEL; EVOLUTION; FEMALE; FERTILITY; GENETICS; INFORMATION PROCESSING; MALE; MATE CHOICE; METHODOLOGY; PHYSIOLOGY; REPRODUCTIVE FITNESS; REVIEW; SEXUAL BEHAVIOR; SPERMATOZOON;

ANIMALS; BIOLOGICAL EVOLUTION; DATA COLLECTION; FEMALE; FERTILITY; GENETIC FITNESS; MALE; MATING PREFERENCE, ANIMAL; MODELS, BIOLOGICAL; SEXUAL BEHAVIOR, ANIMAL; SPERMATOZOA;

MLCS; MLOWN;

EID: 84879490377     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0046     Document Type: Article

References (138)

1. Shuster S, Wade M. 2003 Mating systems and strategies. Princeton, NJ: Princeton University Press.
2. Darwin CR. 1874. The descent of man and selection in relation to sex, 2nd edn. New York, NY: Rand, McNally and Co.
3. Anthes N et al. 2010 Bateman gradients in hermaphrodites: an extended approach to quantify sexual selection. Am. Nat. 173, 249-263. (doi:10. 1086/655218)
4. Pélissié B, Jarne P, David P. 2012 Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite. Evolution 66, 66-81. (doi:10.1111/j.1558-5646. 2011.01442.x)
5. Webster M, Pruett-Jones S, Westneat D, Arnold SJ. 1995 Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49, 1147-1157. (doi:10.2307/2410439)
6. Pitnick S, Hosken DJ, Birkhead TR. 2009 Sperm morphological diversity. In Sperm biology: an evolutionary perspective. (eds TR Birkhead, DJ Hosken, S Pitnick), pp. 69-149. Burlington, MA: Academic Press.
7. Pizzari T, Parker GA. 2009 Sperm competition and the sperm phenotype. In Sperm biology: an evolutionary perspective (eds TR Birkhead, DJ Hosken, S Pitnick), pp. 207-245. Burlington, MA: Academic Press.
8. Parker GA, PIzzari T. 2010 Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934. (doi:10.1111/j.1469-185X.2010.00140.x)
9. Smith RL. 1984 Sperm competition and the evolution of animal mating systems. San Diego, CA: Academic Press.
10. Birkhead T, Møller AP. 1998 Sperm competition and sexual selection. San Diego, CA: Academic Press.
11. Levine L. 1967 Sexual selection in mice. IV. Experimental demonstration of selective fertilization. Am. Nat. 101, 289-294. (doi:10.1086/ 282491)
12. Hotzy C, Arnqvist G. 2009 Sperm competition favors harmful males in seed beetles. Curr. Biol. 19, 404-407. (doi:10.1016/j.cub.2009.01.045)
13. Cheng KM, Siegel PB. 1990 Quantitative genetics of multiple mating. Anim. Behav. 40, 406-407. (doi:10.1016/S0003-3472(05)80939-X)
14. Birkhead T. 1999 Reproductive biology: distinguished sperm in competition. Nature 400, 406-407. (doi:10.1038/22650)
15. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA. 2004 Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr. Biol. 14, 44-47. (doi:10.1016/j.cub. 2003.12.028)
16. García-González F, Simmons LW. 2005 The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J. Evol. Biol. 18, 1097-1103. (doi:10.1111/j.1420-9101.2005.00889.x)
17. Vladić TV, Järvi T. 2001 Sperm quality in the alternative reproductive tactics of Atlantic salmon: the importance of the loaded raffle mechanism. Proc. R. Soc. Lond. B 268, 2375-2381. (doi:10. 1098/rspb.2001.1768)
18. Short RV. 1979 Sex determination and differentiation. Brit. Med. Bull. 35, 121-127.
19. Hosken D, Ward P. 2001 Experimental evidence for testis size evolution via sperm competition. Ecol. Lett. 4, 10-13. (doi:10.1046/j.1461-0248.2001. 00198.x)
20. Wedell N, Gage MJG, Parker GA. 2002 Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313-320. (doi:10.1016/S0169-5347(02)02533-8)
21. Gage MJG, Freckleton RP. 2003 Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc. R. Soc. Lond. B 270, 625-632. (doi:10.1098/rspb. 2002.2258)
22. Pizzari T, Birkhead TR. 2000 Female feral fowl eject sperm of subdominant males. Nature 405, 787-789. (doi:10.1038/35015558)
23. Foster K, Seppä P, Ratnieks FLW, Thorén PA. 1999 Low paternity in the hornet Vespa crabro indicates that multiple mating by queens is derived in vespine wasps. Behav. Ecol. Sociobiol. 46, 252-257. (doi:10.1007/s002650050617)
24. Bartmann S, Gerlach G. 2001 Multiple paternity and similar variance in reproductive success of male and female wood mice (Apodemus sylvaticus) housed in an enclosure. Ethology 107, 889-899. (doi:10. 1046/j.1439-0310.2001.00723.x)
25. Dean MD, Ardlie KG, Nachman MW. 2006 The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol. Ecol. 15, 4141-4151. (doi:10. 1111/j.1365-294X.2006.03068.x)
26. Wade MJ. 1979 Sexual selection and variance in reproductive success. Am.Nat. 114, 742-747. (doi:10.1086/283520)
27. Wade MJ, Arnold SJ. 1980 The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Anim. Behav. 28, 446-461. (doi:10.1016/S0003-3472 (80)80052-2)
28. Bjork A, Pitnick S. 2006 Intensity of sexual selection along the road to isogamy. Nature 441, 742-745. (doi:10.1038/nature04683)
29. Portnoy DS, Piercy AN, Musick JA, Burgess GH, Graves JE. 2007 Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico. Mol. Ecol. 16, 187-197. (doi:10.1111/j. 1365-294X.2006.03138.x)
30. Møller AP, Ninni P. 1998 Review. Sperm competition and sexual selection: a meta-analysis of paternity studies of birds. Behav. Ecol. Sociobiol. 43, 345-358. (doi:10.1007/s002650050501)
31. Pischedda A, Rice WR. 2012 Partitioning sexual selection into its mating success and fertilization success components. Proc. Natl Acad. Sci. USA 109, 2049-2053. (doi:10.1073/pnas.1110841109)
32. Marshall DJ, Evans JP. 2005 The benefits of polyandry in the free-spawning polychaete Galeolaria caespitosa. J. Evol. Biol. 18, 735-741. (doi:10.1111/j.1420-9101.2004.00873.x)
33. Simmons LW, Kvarnemo C. 1997 Ejaculate expenditure by male bushcrickets decreases with sperm competition intensity. Proc. R. Soc. Lond. B 264, 1203-1208. (doi:10.1098/rspb.1997.0166)
34. Simmons LW, Craig M, Llorens T, Schinzig M, Hosken D. 1993 Bushcricket spermatophores vary in accord with sperm competition and parental investment theory. Proc. R. Soc. Lond. B 251, 183-186. (doi:10.1098/rspb.1993.0027)
35. Backus V, Cade WH. 1986 Sperm competition in the field cricket Gryllus integer (Orthoptera: Gryllidae). Fla. Entomol. 69, 722-728. (doi:10. 2307/3495220)
36. Fedorka K, Mousseau TA. 2002 Material and genetic benefits of female multiple mating and polyandry. Anim. Behav. 64, 361-367. (doi:10.1006/anbe. 2002.3052)
37. Bretman A, Newcombe D, Tregenza T. 2009 Promiscuous females avoid inbreeding by controlling sperm storage. Mol. Ecol. 18, 3340-3345. (doi:10.1111/j.1365-294X.2009.04301.x)
38. Pol RG, Casenave JL, Feldhaar H, Milesi FA, Gadau J. 2008 Polyandry in two South American harvester ants. Insect. Soc. 55, 91-97. (doi:10.1007/s00040-007-0975-0)
39. Kellner K, Trindl A, Heinze J, D'Ettorre P. 2007 Polygyny and polyandry in small ant societies. Mol. Ecol. 16, 2363-2369. (doi:10.1111/j.1365-294X. 2007.03297x)
40. Sakurai G, Kasuya E. 2008 Different female mating rates in different populations do not reflect the benefits the females gain from polyandry in the adzuki bean beetle. J. Ethol. 26, 93-98. (doi:10. 1007/s10164-007-0036-1)
41. Tregenza T, Attia F, Bushaiba SS. 2009 Repeatability and heritability of sperm competition outcomes in males and females of Tribolium castaneum. Behav. Ecol. Sociobiol. 63, 817-823. (doi:10.1007/s00265-009-0716-7)
42. Lewis SM, Austad SN. 1990 Sources of intraspecific variation in sperm precedence in red flour beetles. Am. Nat. 135, 351-359. (doi:10.1086/285050)
43. Moya-Larano J, Fox CW. 2006 Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle. Behav. Ecol. 17, 940-946. (doi:10.1093/beheco/arl029)
44. Demary KC, Lewis SM. 2007 Male reproductive allocation in fireflies (Photinus spp.). Invertebr. Biol. 126, 74-80. (doi:10.1111/j.1744-7410.2007. 00078.x)
45. Cook PA, Gage MJG. 1995 Effects of risks of sperm on the numbers competition of eupyrene and apyrene sperm ejaculated by the moth Plodia interpunctella (Lepidoptera: Pyralidae). Behav. Ecol. Sociobiol. 36, 261-268. (doi:10.1007/BF00165835)
46. Dunn DW, Sumner JP, Goulson D. 2005 The benefits of multiple mating to female seaweed flies, Coelopa frigida (Diptera: Coelpidae). Behav. Ecol. Sociobiol. 58, 128-135. (doi:10.1007/s00265-005-0922-x)
47. Frentiu FD, Chenoweth SF. 2008 Polyandry and paternity skew in natural and experimental populations of Drosophila serrata. Mol. Ecol. 17, 1589-96. (doi:10.1111/j.1365-294X.2008.03693.x)
48. Holland B, Rice WR. 1999 Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA 96, 5083-5088. (doi:10.1073/ pnas.96.9.5083)
49. Clark AG, Begun DJ, Prout T. 1999 Female male interactions in drosophila sperm competition. Science 283, 217-220. (doi:10.1126/science.283. 5399.217)
50. Pitnick S, Brown WD, Miller GT. 2001 Evolution of female remating behaviour following experimental removal of sexual selection. Proc. R. Soc. Lond. B 268, 557-563. (doi:10.1098/rspb.2000.1400)
51. Bateman AJ. 1948 Intra-sexual selection in Drosophila. Heredity 2, 349-368. (doi:10.1038/hdy. 1948.21)
52. Gosselin T, Sainte-Marie B, Bernatchez L. 2005 Geographic variation of multiple paternity in the American lobster, Homarus americanus. Mol. Ecol. 14, 1517-1525. (doi:10.1111/j.1365-294X.2005. 02498.x)
53. Jivoff P. 1997 The relative roles of predation and sperm competition on the duration of the postcopulatory association between the sexes in the blue crab, Callinectes sapidus. Behav. Ecol. Sociobiol. 40, 175-185. (doi:10.1007/s002650050331)
54. Todd CD, Stevenson RJ, Reinardy H, Ritchie MG. 2005 Polyandry in the ectoparasitic copepod Lepeophtheirus salmonis despite complex precopulatory and postcopulatory mate-guarding. Mar. Ecol. Prog. Ser. 303, 225-234. (doi:10.3354/ meps303225)
55. Elgar MA, Bruce MJ, Crespigny FECD, Cutler AR, Cutler CL, Gaskett AC, Herberstein ME, Ramamurthy S, Schneider JM. 2003 Male mate choice and patterns of paternity in the polyandrous, sexually cannibalistic orb-web spider, Nephila plumipes. Aust. J. Zool. 51, 357-365. (doi:10.1071/ZO02079)
56. Zeh JA, Newcomer SD, Zeh DW. 1998 Polyandrous females discriminate against previous mates. Proc. Natl Acad. Sci. USA 95, 13732-13736. (doi:10. 1073/pnas.95.23.13732)
57. Harper FM, Hart MW. 2005 Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars. Biol. Bull. 209, 113-126. (doi:10.2307/3593129)
58. Evans JP, Marshall DJ. 2005 Male-by-female interactions influence fertilization success and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution 59, 106-112. (doi:10.1111/j.0014-3820.2005.tb00898.x)
59. Marshall DJ, Evans JP. 2007 Context-dependent genetic benefits of polyandry in a marine hermaphrodite. Biol. Lett. 3, 685-688. (doi:10. 1098/rsbl.2007.0438)
60. Crean AJ, Marshall DJ. 2008 Gamete plasticity in a broadcast spawning marine invertebrate. Proc. Natl Acad. Sci. USA 105, 13508-13513. (doi:10.1073/ pnas.0806590105)
61. Gage MJG, Stockley P, Parker GA. 1995 Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations. Proc. R. Soc. Lond. B 350, 391-399. (doi:10.1098/ rstb.1995.0173)
62. Immler S, Taborsky M. 2009 Sequential polyandry affords post-mating sexual selection in the mouths of cichlid females. Behav. Ecol. Sociobiol. 63, 1219-1230. (doi:10.1007/s00265-009-0744-3)
63. Bechert SA, Magurran AE. 2004 Multiple mating and reproductive skew in Trinidadian guppies. Proc. R. Soc. Lond. B 271, 1009-1014. (doi:10.1098/rspb.2004.2701)
64. King JR, Withler RE. 2005 Male nest site fidelity and female serial polyandry in lingcod (Ophiodon elongatus, Hexagrammidae). Mol. Ecol. 14, 653-660. (doi:10.1111/j.1365-294X.2005.02438.x)
65. DiBattista JD, Feldheim KA, Gruber SH, Hendry AP. 2008 Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks. Mol. Ecol. 17, 783-95. (doi:10.1111/j.1365-294X.2007.03623.x)
66. Fuller RC. 1998 Sperm competition affects male behaviour and sperm output in the rainbow darter. Proc. R. Soc. Lond. B 265, 2365-2371. (doi:10. 1098/rspb.1998.0585)
67. Spence R, Smith C. 2006 Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav. Ecol. 17, 779-783. (doi:10.1093/beheco/arl016)
68. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S. 2009 Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc. Natl Acad. Sci. USA 106, 1128-1132. (doi:10.1073/pnas.0809990106)
69. Roberts J, Standish R, Byrne P, Doughty P. 1999 Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim. Behav. 57, 721-726. (doi:10.1006/anbe.1998.1019)
70. Sztatecsny M, Jehle R, Burke T, Hödl W. 2006 Female polyandry under male harassment: the case of the common toad (Bufo bufo). J. Zool. 270, 517-522. (doi:10.1111/j.1469-7998.2006.00120.x)
71. Stille B, Madsen T, Niklasson M, Nikiasson M. 1986 Multiple paternity in the adder, Vipera berus. Oikos 47, 173-175. (doi:10.2307/3566042)
72. Fantin C, Viana LS, Monjeló LADS, Farias IP. 2008 Polyandry in Podocnemis unifilis (Pleurodira; Podocnemididae), the vulnerable yellow-spotted Amazon River turtle. Amphibia-Reptilia 29, 479-486. (doi:10.1163/156853808786230361)
73. Eizaguirre C, Laloi D, Massot M, Richard M, Federici P, Clobert J. 2007 Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard. Proc. R. Soc. B 274, 425-430. (doi:10.1098/rspb.2006.3740)
74. Lee PLM, Hays GC. 2004 Polyandry in a marine turtle: females make the best of a bad job. Proc. Natl Acad. Sci. USA 101, 6530-6535. (doi:10.1073/ pnas.0307982101)
75. Kissner KJ, Weatherhead PJ, Gibbs HL. 2005 Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon. Behav. Ecol. Sociobiol. 59, 207-214. (doi:10.1007/s00265-005-0026-7)
76. Moore JA, Nelson NJ, Keall SN, Daugherty CH. 2008 Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara). Conserv. Genet. 9, 1243-1251. (doi:10.1007/s10592-007-9452-6)
77. Prosser MR, Weatherhead PJ, Gibbs HL, Brown GP. 2002 Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon). Behav. Ecol. 13, 800-807. (doi:10.1093/beheco/13.6.800)
78. Dietrich V, Schmoll T, Winkel W, Epplen J, Lubjuhn T. 2004 Pair identity: an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141, 817-835. (doi:10. 1163/1568539042265644)
79. Burke T, Davies NB, Bruford MW, Hatchwell BJ. 1989 Parental care and mating related to paternity by DNA fingerprinting related to paternity by DNA fingerprinting. Nature 338, 249-251. (doi:10.1038/ 338249a0)
80. Faaborg J, Parker PG, DeLay L, de Vries T, Bednarz JC, Paz SM, Naranjo J, Waite TA. 1995 Confirmation of cooperative polyandry in the Galapagos hawk (Buteo galapagoensis). Behav. Ecol. Sociobiol. 36, 83-90. (doi:10.1007/BF00170712)
81. Heinsohn R, Ebert D, Legge S, Peakall R. 2007 Genetic evidence for cooperative polyandry in reverse dichromatic Eclectus parrots. Anim. Behav. 74, 1047-1054. (doi:10.1016/j.anbehav.2007.01.026)
82. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT. 2009 Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63, 2466-2473. (doi:10. 1111/j.1558-5646.2009.00725.x)
83. Whittingham LA, Dunn PO, Magrath RD. 1997 Relatedness, polyandry and extra-group paternity in the cooperatively-breeding white-browed scrubwren (Sericornis frontalis). Behav. Ecol. Sociobiol. 40, 261-270. (doi:10.1007/s002650050341)
84. Piper WH, Slater G. 1993 Polyandry and incest avoidance in the cooperative stripe-backed wren of Venezuela. Behaviour 3, 227-247. (doi:10.1163/ 156853993X00597)
85. Dunn PO, Robertson RJ, Michaud-Freeman D, Boag PT. 1994 Extra-pair paternity in tree swallows: why do females mate with more than one male? Behav. Ecol. Sociobiol. 35, 273-281. (doi:10.1007/ BF00170708)
86. 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)
87. Carmichael LE, Szor G, Berteaux D, Giroux MA, Cameron C, Strobeck C. 2007 Free love in the far north: plural breeding and polyandry of arctic foxes (Alopex lagopus) on Bylot Island, Nunavut. Can. J. Zool. 85, 338-343. (doi:10.1139/Z07-014)
88. Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A. 2006 Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild. Nature 444, 89-92. (doi:10.1038/nature05206)
89. Kraaijeveld-Smit F, Ward S, Smith PT. 2002 Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behav. Ecol. Sociobiol. 52, 84-91. (doi:10.1007/ s00265-002-0485-z)
90. Keane B, Waser PM, Creel S, Creel NM, Elliott JF, Minchella DJ. 1994 Subordinate reproduction in dwarf mongooses. Anim. Behav. 47, 65-75. (doi:10.1006/anbe.1994.1008)
91. Baker A, Dietz JM, Kleiman DG. 1993 Behavioral evidence for monopolization of paternity in multimale groups of golden lion tamarins. Anim. Behav. 46, 1091-1103. (doi:10.1006/anbe.1993.1299)
92. Baker RJ, Makova KD, Chesser RK. 1999 Microsatellites indicate a high frequency of multiple paternity in Apodemus (Rodentia). Mol. Ecol. 8, 107-111. (doi:10.1046/j.1365-294X.1999.00541.x)
93. Booth W, Montgomery WI, Prodöhl PA. 2007 Polyandry by wood mice in natural populations. J. Zool. 273, 176-182. (doi:10.1111/j.1469-7998. 2007.00312.x)
94. Arnold SJ. 1994 Bateman's principles and the measurement of sexual selection in plants and animals. Am. Nat. 144, S126-S149. (doi:10.1086/ 285656)
95. Arnold SJ, Duvall D. 1994 Animal mating systems: a synthesis based on selection theory. Am. Nat. 143, 317-348. (doi:10.1086/285606)
96. Shuster S. 2009 Sexual selection and mating systems. Proc. Natl Acad. Sci. USA 106, 10009-10 016.
97. Parker G. 1970 Sperm competition and its evolutionary consequences in the insects. Biol. Rev. Cambr. Philos. Soc. 45, 525-567. (doi:10.1111/j. 1469-185X.1970.tb01176.x)
98. Lewis S, Austad S. 1994 Sexual selection in flour beetles: the relationship between sperm precedence and male olfactory attractiveness. Behav. Ecol. 5, 223-224. (doi:10.1093/beheco/5.2.223)
99. Clark AG, Aguade M, Prout T, Harshmad LG, Langley CH. 1995 Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139, 189-201. (doi:10.1073/pnas.0901132106)
100. Wade M. 1987 Measuring sexual selection. In Sexual selection: testing the alternatives (eds JW Bradbury, MB Andersson), pp. 197-207. New York, NY: John Wiley and Sons.
101. Wade MJ, Shuster SM. 2005 Don't throw Bateman out with the bathwater! Integr. Comp. Biol. 45, 945-51. (doi:10.1093/icb/45.5.945)
102. Crow JF. 1958 Some possibilities for measuring selection intensities in man. Hum. Biol. 30, 1-13.
103. Jones AG. 2009 On the opportunity for sexual 26 selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution 63, 1673-1684. (doi:10.1111/j.1558-5646.2009.00664.x)
104. Wade MJ, Shuster SM. 2004 Sexual selection: harem size and the variance in male reproductive success. Am. Nat. 164, E83-E89. (doi:10.1086/424531)
105. Shuster SM. 2010 Alternative mating strategies. In Evolutionary behavioral ecology (eds C Fox, DF Westneat), pp. 434-450. Cambridge, UK: Cambridge University Press.
106. Trivers RL. 1972 Parental investment and sexual selection. In Sexual selection and the descent of man (ed. B Campbell), pp. 136-179. Chicago, IL: Aldine Press.
107. Levitan DR, Petersen CW. 1995 Sperm limitation in the sea. Trends. Ecol. Evol. 10, 228-231. (doi:10. 1016/S0169-5347(00)89071-0)
108. Weddell N, Gage MJG, Parker GA. 2002 Sperm competition, male prudence and sperm-limited females. Trends. Ecol. Evol. 17, 313-320. (doi:10. 1016/S0169-5347(02)02533-8)
109. Mays HL, Albrecht T, Liu M, Hill GE. 2008 Female choice for genetic complementarity in birds: a review. Genetica 134, 147-58. (doi:10.1007/ s10709-007-9219-5)
110. Newcomer SD, Zeh JA, Zeh DW. 1999 Genetic benefits enhance the reproductive success of polyandrous females. Proc. Natl. Acad. Sci. USA 96, 10236-10241. (doi:10.1073/pnas.96.18.10236)
111. Eberhard WG. 1996 Females in control: sexual selection by cryptic female choice. Princeton, NJ: Princeton University Press.
112. Jones AG, Ardren WR. 2003 Methods of parentage analysis in natural populations. Mol. Ecol. 12, 2511-2523. (doi:10.1046/j.1365-294X. 2003.01928.x)
113. Bernasconi G, Keller L. 2001 Female polyandry affects their sons' reproductive success in the red flour beetle Tribolium castaneum. J. Evol. Biol. 14, 186-193. (doi:10.1046/j.1420-9101.2001.00247.x)
114. Byrne PG, Whiting MJ. 2008 Simultaneous polyandry increases fertilization success in an African foam-nesting treefrog. Anim. Behav. 76, 1157-1164. (doi:10.1016/j.anbehav.2008.05.019)
115. Byrne PG, Keogh JS. 2009 Extreme sequential polyandry insures against nest failure in a frog. Proc. R. Soc. B 276, 115-120. (doi:10.1098/rspb.2008.0794)
116. Foltz ADW, Schwagmeyer PL. 1989 Sperm competition in the thirteen-lined ground squirrel: differential fertilization success under field conditions. Am. Nat. 133, 257-265. (doi:10.1086/ 284914)
117. Kaitala A, Wiklund C. 1994 Polyandrous female butterflies forage for matings. Behav. Ecol. Sociobiol. 35, 385-388. (doi:10.1007/BF00165840)
118. Tregenza T, Wedell N. 1998 Benefits of multiple mates in the cricket Gryllus bimacculatus. Evolution 52, 1726-1730. (doi:10.2307/2411345)
119. 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)
120. Pearse DE, Janzen FJ, Avise JC. 2002 Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav. Ecol. Sociobiol. 51, 164-171. (doi:10.1007/s00265-001-0421-7)
121. Murie JO. 1995 Mating behavior of Columbian ground squirrels. I. Multiple mating by females and multiple paternity. Can. J. Zool. 73, 1819-1926. (doi:10.1139/z95-214)
122. Simmons LW. 2001 The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J. Evol. Biol. 14, 585-594. (doi:10.1046/j.1420-9101.2001.00309.x)
123. Burpee D, Sakaluk SK. 1993 Repeated matings offset costs of reproduction in female crickets. Evol. Ecol. 7, 240-250. (doi:10.1007/ BF01237742)
124. Ivy TM, Sakaluk SK, Url S. 2005 Polyandry promotes enhanced offspring survival in decorated crickets. Evolution 59, 152-159. (doi:10.1111/j.0014-3820. 2005.tb00902.x)
125. Ronkainen K, Kaitala A, Kivelä SM. 2010 Polyandry, multiple mating, and female fitness in a water strider Aquarius paludum. Behav. Ecol. Sociobiol. 64, 657-664. (doi:10.1007/s00265-009-0883-6)
126. 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)
127. Liu X-P, He H-M, Kuang X-J, Xue F-S. 2010 A comparison of female fitness between monogamy and polyandry in the cabbage beetle, Colaphellus bowringi. Anim. Behav. 79, 1390-1395. (doi:10. 1016/j.anbehav.2010.03.019)
128. Drnevich JM, Papke RS, Rauser CL, Rutowski RL. 2001 Material benefits from multiple mating in female mealworm beetles (Tenebrio molitor L.). J. Insect Behav. 14, 215-230. (doi:10.1023/A:1007889712054)
129. Svard L, McNeil JN. 1994 Female benefit, male rick: polyandry in the true armyworm Pseudaletia unipuncta. Behav. Ecol. Sociobiol. 35, 319-326. (doi:10.1016/S0022-1910(98)00137-1)
130. McNamara KB, Elgar MA, Jones TM. 2008 A longevity cost of re-mating but no benefits of polyandry in the almond moth, Cadra cautella. Behav. Ecol. Sociobiol. 62, 1433-1440. (doi:10. 1007/s00265-008-0573-9)
131. Uhl G, Schmitt S, Schäfer MA. 2005 Fitness benefits of multiple mating versus female mate choice in the cellar spider (Pholcus phalangioides). Behav. Ecol. Sociobiol. 59, 69-76. (doi:10.1007/s00265-005-0010-2)
132. Martin OY, Demont M. 2008 Reproductive traits: Evidence for sexually selected sperm. Curr. Biol. 18, R79-R81. (doi:10.1016/j.cub.2007.11.031)
133. Myers EM, Zamudio KR. 2004 Multiple paternity in 27 an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success. Mol. Ecol. 13, 1951-1963. (doi:10.1111/j.1365-294X.2004.02208.x)
134. Wolf JB, Wade MJ. 2001 On the assignment of fitness to parents and offspring: whose fitness is it and when does it matter? J. Evol. Biol. 14, 347-356. (doi:10.1046/j.1420-9101.2001.00277.x)
135. Wade M. 1998 The evolutionary genetics of maternal effects. In Maternal effects as adaptations (eds T Mousseau, C Fox), pp. 5-21. Oxford, UK: Oxford University Press.
136. 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)
137. Shuker DM, Phillimore AJ, Burton-Chellew MN, Hodge SE, West SA. 2007 The quantitative genetic basis of polyandry in the parasitoid wasp, Nasonia vitripennis. Heredity 98, 69-73. (doi:10.1038/sj.hdy.6800897)
138. Halliday T, Arnold S. 1987 Multiple mating by females: a perspective from quantitative genetics. Anim. Behav. 35, 939-941. (doi:10.1016/S0003-3472(87)80138-0)