The dynamic relationship between polyandry and selfish genetic elements

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 368, Issue 1613, 2013, Pages

  Wedell, Nina ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Sex ratio distorter; Sexual conflict; Sperm competition; Wolbachia

Indexed keywords

EUKARYOTE; FERTILIZATION (REPRODUCTION); FISH; GENETIC ANALYSIS; GENOME; MATING BEHAVIOR; MICROBIAL ACTIVITY; POLYANDRY; SPERM COMPETITION;

BACTERIA (MICROORGANISMS); EUKARYOTA; WOLBACHIA;

ANIMAL; BIOLOGICAL MODEL; CONFLICT; EVOLUTION; FEMALE; FERTILITY; GENETICS; MALE; MATE CHOICE; NUCLEOTIDE REPEAT; PHYSIOLOGY; POPULATION GENETICS; REVIEW; SEX RATIO; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT;

ANIMALS; BIOLOGICAL EVOLUTION; CONFLICT (PSYCHOLOGY); FEMALE; FERTILITY; GENETICS, POPULATION; MALE; MATING PREFERENCE, ANIMAL; MODELS, BIOLOGICAL; REPETITIVE SEQUENCES, NUCLEIC ACID; SEX CHARACTERISTICS; SEX RATIO; SEXUAL BEHAVIOR, ANIMAL;

MLCS; MLOWN;

EID: 84879468501     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2012.0049     Document Type: Review

References (102)

1. Birkhead TR, Møller AP. 1998 Sperm competition and sexual selection. London, UK: Academic Press.
2. Birkhead TR, Hosken DJ, Pitnick S. 2009 Sperm biology: an evolutionary perspective. Burlington, MA: Academic Press.
3. Lima SL, Dill LM. 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640. (doi:10. 1139/z90-092)
4. Crudgington HS, Siva-Jothy MT. 2000 Genital damage, kicking and early death. Nature 407, 855-856. (doi:10.1038/35038154)
5. Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L. 1995 Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241-244. (doi:10.1038/373241a0)
6. Hurst GDD, Sharpe RG, Broomfield AH, Walker LE, Majerus TMO, Zakharov IA, Majerus MEN. 1995 Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecol. Entomol. 20, 230-236. (doi:10.1111/j.1365-2311. 1995.tb00452.x)
7. Davies NB, Hartley IR, Hatchwell BJ, Langmore NE. 1996 Female control of copulations to maximize male help: a comparison of polygynandrous alpine accentors, Prunella collaris, and dunnocks, P. modularis. Anim. Behav. 51, 27-47. (doi:10. 1006/anbe.1996.0003)
8. 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)
9. 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)
10. Parker GA, Pizzari T. 2010 Sperm competition and ejaculate economics. Biol. Rev. 85, 897-934. (doi:10.1111/j.1469-185X.2010.00140.x)
11. Clutton-Brock TH. 1989 Review lecture: mammalian mating systems. Proc. R. Soc. Lond. B 236, 339-372. (doi:10.1098/rspb.1989.0027)
12. 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)
13. 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)
14. Hosken DJ, Taylor ML, Hoyle K, Higgins S, Wedell N. 2008 Attractive males have greater success in sperm competition. Curr. Biol. 18, R553-R554. (doi:10.1016/j.cub.2008.04.028)
15. 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)
16. 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)
17. Pryke SR, Rollins LA, Griffith SC. 2010 Females use multiple mating and genetically loaded sperm competition to target compatible genes. Science 329, 964-967. (doi:10.1126/science.1192407)
18. Tregenza T, Wedell N. 2002 Polyandrous females avoid costs of inbreeding. Nature 415, 71-73. (doi:10.1038/415071a)
19. 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)
20. Zeh JA, Zeh DW. 1997 The evolution of polyandry. II. Post-copulatory defences against genetic incompatibility. Proc. R. Soc. Lond. B 264, 69-75. (doi:10.1098/rspb.1997.0010)
21. Tregenza T, Wedell N. 2000 Genetic compatibility, mate choice, and patterns of parentage. Mol. Ecol. 9, 1013-1027. (doi:10.1046/j.1365-294x.2000.00964.x)
22. Ayroles JF, Hughes KA, Rowe KC, Reedy MM, Rodriguez-Zas SL, Drnevich JM, Cáceres CE, Paige KN. 2009 A genomewide assessment of inbreeding depression: gene number, function, and mode of action. Conserv. Biol. 23, 920-930. (doi:10.1111/j.1523-1739.2009.01186.x)
23. Zeh JA, Zeh DW. 1996 The evolution of polyandry. I. Intra-genomic conflict and genetic incompatibility. Proc. R. Soc. Lond. B 263, 1711-1717. (doi:10. 1098/rspb.1996.0250)
24. Arnqvist G, Rowe L. 2005 Sexual conflict. Princeton, NJ: Princeton University Press.
25. Hrdy SB. 1979 Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 13-40. (doi:10.1016/0162-3095(79) 90004-9)
26. Jaffe R, Moritz RFA, Kraus FB. 2009 Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii. Popul. Ecol. 51, 227-236. (doi:10.1007/s10144-008-0133-1)
27. Rankin D, Dieckmann U, Kokko H. 2011 Sexual conflict and the tragedy of the commons. Am. Nat. 177, 780-791. (doi:10.1086/659947)
28. Price TAR, Hurst GDD, Wedell N. 2010 Polyandry prevents extinction. Curr. Biol. 20, 471-475. (doi:10.1016/j.cub.2010.01.050)
29. Simmons LW. 2005 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)
30. Hosken DJ, Stockley P, Tregenza T, Wedell N. 2009 Monogamy and the battle of the sexes. Ann. Rev. Entomol. 54, 361-378. (doi:10.1146/annurev.ento.54.110807.090608)
31. Trivers RL. 1974 Parent-offspring conflict. Am. Zool. 14, 249-264. (doi:10.1093/icb/14.1.249)
32. Hughes WO, Oldroyd BP, Beekman M, Ratnieks LW. 2008 Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320, 1213-1216. (doi:10.1126/science.1156108)
33. Cornwallis CK, West SA, Davis KE, Griffin AS. 2010 Promiscuity and the evolutionary transition to complex societies. Nature 466, 969-972. (doi:10.1038/nature09335)
34. Haig D, Bergstrom CT. 1995 Multiple mating, sperm competition and meiotic drive. J. Evol. Biol. 8, 265-282. (doi:10.1046/j.1420-9101.1995.8030265.x)
35. 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)
36. 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)
37. Price TAR, Wedell N. 2008 Selfish genetic elements and sexual selection: their impact on male fertility. Genetica 132, 295-307. (doi:10.1007/s10709-007-9173-2)
38. Lewis Z, Price TAR, Wedell N. 2008 Review: sperm competition, immunity, selfish genes and cancer. Cell Mol. Life Sci. 65, 3241-3254. (doi:10.1007/s00018-008-8238-4)
39. Champion de Crespigny FE, Wedell N. 2006 Wolbachia infection reduces sperm competitive ability in an insect. Proc. R. Soc. B 273, 1455-1458. (doi:10.1098/rspb.2006.3478)
40. Price TAR, Bretman AJ, Avent TD, Snook RR, Hurst GDD, Wedell N. 2008 Sex ratio distorter reduces sperm competitive ability in an insect. Evolution 62, 1644-1652. (doi:10.1111/j.1558-5646.2008.00386.x)
41. Burt A, Trivers RL. 2006 Genes in conflict: the biology of selfish genetic elements. Harvard, MA: Harvard University Press.
42. Hurst GDD, Werren JH. 2001 The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2, 597-606. (doi:10.1038/35084545)
43. Werren JH. 2011 Selfish genetic elements, genetic conflict, and evolutionary innovation. Proc. Natl Acad. Sci. USA 108(Suppl. 2), 10863-10870. (doi:10.1073/pnas.1102343108)
44. Jaenike J. 2001 Sex chromosome meiotic drive. Ann. Rev. Ecol. Syst. 32, 25-49. (doi:10.1146/annurev.ecolsys.32.081501.113958)
45. Haig D. 2012 Retroviruses and the placenta. Curr. Biol. 22, R609-R613. (doi:10.1016/j.cub.2012.06.002)
46. Wilkinson GS, Presgraves DC, Crymes L. 1998 Male eye span in stalk-eyed flies indicates genetic quality by meiotic drive suppression. Nature 391, 276-279. (doi:10.1038/34640)
47. Lenington S. 1991 The t-complex: a story of genes, behavior, and populations. Adv. Stud. Behav. 20, 51-86. (doi:10.1016/S0065-3454 (08)60319-8)
48. Miller W, Ehrman L, Schneider D. 2010 Infection speciation revisited: impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Path. 6, 1001214. (doi:10.1371/journal.ppat.1001214)
49. Sharon G, Segal D, Ringo JM, Hefetz A, Zilber-Rosenberg I, Rosenberg E. 2010 Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 107, 20051-20056. (doi:10.1073/pnas.1009906107)
50. Ringo J, Sharon G, Segal D. 2011 Bacteria-induced sexual isolation in Drosophila. Fly 5, 310-315. (doi:10.4161/fly.5.4.15835)
51. Vala F, Breeuwer JAJ, Sabelis MW. 2004 Endosymbiont associated assortative mating in a spider mite. J. Evol. Biol. 17, 692-700. (doi:10.1046/j.1420-9101.2003.00679.x)
52. Moureau J, Rigaut T. 2003 Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite-induced excess of females? Proc. R. Soc. Lond. B 270, 1535-1540. (doi:10.1098/rspb.2003.2402)
53. Dunn AM, Andrews T, Ingrey H, Riley J, Wedell N. 2006 Strategic sperm allocation under parasitic sexratio distortion. Biol. Lett. 2, 78-80. (doi:10.1098/rsbl.2005.0402)
54. Champion de Crespigny FE, Wedell N. 2007 Mate preferences in Drosophila infected with Wolbachia? Behav. Ecol. Sociolbiol. 61, 1229-1235. (doi:10.1007/s00265-007-0353-y)
55. Markov AV, Lazebny OE, Goryacheva II, Antipin MI, Kulikov AM. 2009 Symbiotic bacteria affect mating choice in Drosophila melanogaster. Anim. Behav. 77, 1011-1017. (doi:10.1016/j.anbehav.2009.01.011)
56. Fernandez AA, Morris MR. 2008 Mate choice for more melanin as a mechanism to maintain a functional oncogene. Proc. Natl Acad. Sci. USA 105, 13503-13507. (doi:10.1073/pnas.0803851105)
57. Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N. 2012 No evidence of mate discrimination against males carrying a sex ratio distorter in Drosophila pseudoobscura. Behav. Ecol. Sociobiol. 66, 561-568. (doi:10.1007/s00265-011-1304-1)
58. Nichols RA, Butlin RK. 1989 Does runaway sexual selection work in finite populations. J. Evol. Biol. 2, 299-313. (doi:10.1046/j.1420-9101.1989.2040299.x)
59. Johns PM, Wolfenbarger LL, Wilkinson GS. 2005 Genetic linkage between a sexually selected trait and X chromosome meiotic drive. Proc. R. Soc. B 272, 2097-2103. (doi:10.1098/rspb.2005.3183)
60. Lenington S, Coopersmith C, Williams J. 1992 Genetic basis of mating preferences in wild house mice. Am. Zool. 32, 40-47. (doi:10.1093/icb/32.1.40)
61. Snook RR, Cleland SY, Wolfner MF, Karr TL. 2000 Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155, 167-178.
62. Lewis Z, Champion de Crespigny FE, Sait SM, Tregenza T, Wedell N. 2011 Wolbachia infection lowers fertile sperm transfer in a moth. Biol. Lett. 7, 187-189. (doi:10.1098/rsbl.2010.0605)
63. Policansky D, Ellison J. 1970 'Sex ratio' in Drosophila pseudoobscura: spermiogenic failure. Science 169, 888-889. (doi:10.1126/science.169.3948.888)
64. 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)
65. Dyson EA, Hurst GDD. 2004 Persistence of an extreme sex-ratio bias in a natural population. Proc. Natl Acad. Sci. USA 101, 6520-6523. (doi:10. 1073/pnas.0304068101)
66. Charlat S, Reuter M, Dyson EA, Hornett EA, Duplouy AMR, Davies N, Roderick GK, Wedell N, Hurst GDD. 2007 Male killing bacteria trigger a cycle of increasing male fatigue and female promiscuity. Curr. Biol. 17, 273-277. (doi:10.1016/j.cub.2006.11.068)
67. Policansky D, Dempsey B. 1978 Modifiers and 'sexratio' in Drosophila pseudoobscura. Evolution 32, 922-924. (doi:10.2307/2407507)
68. Powell J. 1997 Progress and prospects in evolutionary biology: the Drosophila model. Oxford, UK: Oxford University Press.
69. 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)
70. Manser A, Lindholm A, König B, Bagheri H. 2011 Polyandry and the decrease of a selfish genetic element in a wild house mouse population. Evolution 65, 2435-2447. (doi:10.1111/j.1558-5646.2011.01336.x)
71. Lawson LP, Vander Meer RK, Shoemaker D. 2012 Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta. Proc. R. Soc. B 279, 3217-3222. (doi:10.1098/rspb.2012.0315)
72. Zeh JA, Zeh DW. 2003 Toward a new sexual selection paradigm: polyandry, conflict and incompatibility. Ethology 109, 929-950. (doi:10.1046/j.1439-0310.2003.00945.x)
73. Wilkinson GS, Swallow JG, Christensen SJ, Madden K. 2003 Phylogeography of sex ratio and multiple mating in stalk-eyed flies from Southeast Asia. Genetica 117, 37-46. (doi:10.1023/A:1022360531703)
74. Fry CL, Wilkinson GS. 2004 Sperm survival in female stalkeyed flies depends on seminal fluid and meiotic drive. Evolution 58, 1622-1626.
75. Goodacre SL, Martin OY. 2012 Modification of insect and arachnid behaviours by vertically transmitted endosymbionts: infections as drivers of behavioural change and evolutionary novelty. Insects 3, 246-261. (doi:10.3390/insects3010246)
76. Jiggins FM, Hurst GDD, Majerus MEN. 2000 Sexratio distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. R. Soc. Lond. B 267, 69-73. (doi:10.1098/rspb.2000.0968)
77. Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N. 2010 Sex ratio drive promotes sexual conflict and sexual coevolution in the fly Drosophila pseudoobscura. Evolution 64, 1504-1509.
78. Moreau J, Bertin A, Caubet Y, Rigaud T. 2001 Sexual selection in an isopod with Wolbachia-induced sexual reversal: males prefer real females. J. Evol. Biol. 14, 388-394. (doi:10.1046/j.1420-9101.2001.00292.x)
79. Marshall JL. 2007 Rapid evolution of spermathecal duct length in the Allonemobius socius complex of crickets: species, population and Wolbachia effects. PLoS ONE 2, e720. (doi:10.1371/journal.pone.0000720)
80. Miller GT, Pinick S. 2002 Sperm-female coevolution in Drosophila. Science 298, 1230-1233. (doi:10. 1126/science.1076968)
81. Hayashi TI, Marshall JL, Gavrilets S. 2007 The dynamics of sexual conflict over mating rate with endosymbiont infection that affects reproductive phenotypes. J. Evol. Biol. 20, 2154-2164. (doi:10.1111/j.1420-9101.2007.01429.x)
82. Champion de Crespigny FE, Pitt T, Wedell N. 2006 Increased male mating rate in Drosophila is associated with Wolbachia infection. J. Evol. Biol. 19, 1964-1972. (doi:10.1111/j.1420-9101.2006.01143.x)
83. Karr TL, Yang W, Feder ME. 1998 Overcoming cytoplasmic incompatibility in Drosophila. Proc. R. Soc. Lond. B 265, 391-395. (doi:10.1098/rspb.1998.0307)
84. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. 2008 Wolbachia and virus protection in insects. Science 322, 702. (doi:10.1126/science.1162418)
85. Teixeira L, Ferreira A, Ashburner M. 2008 The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6, 2753-2763. (doi:10.1371/journal.pbio.1000002)
86. Longdon B, Fabian DK, Hurst GDD, Jiggins FM. 2012 Male-killing Wolbachia do not protect Drosophila bifasciata against viral infection. BMC Microbiol. 12, S8. (doi:10.1186/1471-2180-12-S1-S8)
87. Taylor DR, Jaenike J. 2002 Sperm competition and the dynamics of X chromosome drive: stability and extinction. Genetics 160, 1721-1751.
88. Silver LM. 1993 The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet. 9, 250-254. (doi:10.1016/0168-9525(93)90090-5)
89. Carroll L, Meagher S, Morrison L, Penn D, Potts W. 2004 Fitness effects of a selfish gene (the Mus t complex) are revealed in an ecological context. Evolution 58, 1318-1328.
90. Carvalho AB, Vaz CS. 1999 Are Drosophila SR drive chromosomes always balanced? Heredity 83, 221-228. (doi:10.1038/sj.hdy.6886100)
91. Dyer K. 2011 Local selection underlies the geographic distribution of sex-ratio drive in Drosophila neotestacea. Evolution 66, 973-984. (doi:10.1111/j.1558-5646.2011.01497.x)
92. Toju H, Fukatsu T. 2011 Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol. Ecol. 20, 853-868. (doi:10.1111/j.1365-294X.2010.04980.x)
93. Smith DT, Hosken DJ, Rostant WG, Griffin RM, Bretman A, Price TAR, ffrench-Constant RH, Wedell N. 2011 DDT resistance, epistasis and male fitness in flies. J. Evol. Biol. 24, 1351-1362. (doi:10.1111/j.1420-9101.2011.02271.x)
94. McCart C, Buckling A, ffrench-Constant RH. 2005 DDT resistance in flies carries no cost. Curr. Biol. 15, R587-R589. (doi:10.1016/j.cub.2005.07.054)
95. Catania F, Kauer MO, Daborn PJ, Yen JL, ffrench-Constant RH, Schlotterer C. 2004 World wide survey of an Accord insertion and its association with DDT resistance in Drosophila melanogaster. Mol. Ecol. 13, 2491-2504. (doi:10.1111/j.1365-294X.2004.02263.x)
96. Presgraves DC. 2010 The molecular evolutionary basis of species formation. Nat. Rev. Gen. 11, 175-180. (doi:10.1038/nrg2718)
97. Phadnis N, Orr HAA. 2008 A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science 323, 376-379. (doi:10. 1126/science.1163934)
98. Taylor DR, Ingvarson PK. 2003 Common features of segregation distortion in plants and animals. Genetica 117, 27-35. (doi:10.1023/A:102230 8414864)
99. Kaneshiro KY. 2006 Sexual selection in the Hawaiian Drosophillidae. Proc. Hawaiian Entomol. Soc. 38, 1-19.
100. Tinghitella RM, Zuk M. 2009 Asymmetric mating preferences accommodated the rapid evolutionary loss of a sexual signal. Evolution 63, 2087-2098. (doi:10.1111/j.1558-5646.2009.00698.x)
101. Cornell SJ, Tregenza T. 2007 A new theory for the evolution of polyandry as a means of inbreeding avoidance. Proc. R. Soc. B 274, 2873-2879. (doi:10.1098/rspb.2007.0926)
102. Price TAR, Lewis Z, Smith DT, Hurst GDD, Wedell N. 2011 Remating in the laboratory reflects rates of polyandry in the wild. Anim. Behav. 82, 1381-1386. (doi:10.1016/j.anbehav.2011.09.022)