Abstract
Females of many species mate with more than one male (polyandry), yet the adaptive significance of polyandry is poorly understood. One hypothesis to explain the widespread occurrence of multiple mating is that it may allow females to utilize post-copulatory mechanisms to reduce the risk of fertilizing their eggs with sperm from incompatible males. Selfish genetic elements (SGEs) are ubiquitous in eukaryotes, frequent sources of reproductive incompatibilities, and associated with fitness costs. However, their impact on sexual selection is largely unexplored. In this review we examine the link between SGEs, male fertility and sperm competitive ability. We show there is widespread evidence that SGEs are associated with reduced fertility in both animals and plants, and present some recent data showing that males carrying SGEs have reduced paternity in sperm competition. We also discuss possible reasons why male gametes are particularly vulnerable to the selfish actions of SGEs. The widespread reduction in male fertility caused by SGEs implies polyandry may be a successful female strategy to bias paternity against SGE-carrying males.
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Allen JF (1996) Separate sexes and the mitochondrial theory of ageing. J Theor Biol 180:135–140
Andersson M (1994) Sexual Selection. Princeton University Press, Princeton
Arnqvist G, Rowe L (2005) Sexual Conflict. Princeton University Press, Princeton
Artz K, Shin H-S, Bennet D (1982) Gene mapping within the T/t complex of the mouse. II. Anomalous position of the H-2 complex in t haplotypes. Cell 28:471–476
Atlan A, Joly D, Capillon C, Montchamp-Moreau C (2004) Sex-ratio distorter of Drosophila simulans reduces male productivity and sperm competition ability. J Evol Biol 17:744–751
Beckenbach AT (1996) Selection and the “sex-ratio” polymorphism in natural populations of Drosophila pseudoobscura. Evolution 50:787–794
Beukeboom LW (1994) Phenotypic fitness effects on the selfish B-chromosome, paternal sex-ratio (PSR) in the parasitic wasp Nasonia vitripennis. Evol Ecol 8:1–24
Birkhead TR, Møller AP (1998) Sperm Competition and Sexual Selection. Academic Press
Burt A, Trivers R (2006) Genes in Conflict: the Biology of Selfish Genetic Elements. Harvard University Press, Harvard
Capillon C, Atlan A (1999) Evolution of driving X chromosomes and resistance factors in experimental populations of Drosophila simulans. Evolution 53:506–517
Carvalho AB (2002) Origin and evolution of the Drosophila Y chromosome. Curr Opin Genet Dev 12:664–668
Champion de Crespigny FE, Butlin RK, Wedell N (2005) Can cytoplasmic incompatibility inducting Wolbachia promote the evolution of mate preferences? J Evol Biol 18:967–977
Champion de Crespigny FE, Wedell N (2006) Wolbachia infection reduces sperm competitive ability in an insect. Proc R Soc B 273:1455–1458
Champion de Crespigny FE, Wedell N (2007) Mate preferences in Drosophila infected with Wolbachia? Behav Ecol Sociobiol 61:1229–1235
Chance B, Sies H, Boveris A (1979) Hydroperoxide metabolism in mammalian organs. Physiol Rev 59:527–605
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
Chen CB, Marcus A, Li WX, Hu Y, Calzada JPV, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409
Condamine H, Guenet J-L, Jacob F (1983) Recombination between two mouse t-haplotypes (tw12tf and tLub-1): segregation of lethal factors relative to centromere and tufted locus. Genet Res 42:335–344
Crespi BJ, Summers K (2006) Positive selection in the evolution of cancer. Biol Rev 81:407–424
Curtsinger JW, Feldman MW (1980) Experimental and theoretical analyses of the “sex ratio’ polymorphism in Drosophila pseudoobscura. Genetics 94:445–466
Darwin CR (1877) The different forms of flowers on plants of the same species. Murray, London
Dermitzakis ET, Masly JP, Waldrip HM, Clark AG (2000) Non-Mendelian segregation of sex chromosomes in heterospecific Drosophila males. Genetics 154:687–694
Dobzhansky T, Epling C (1944) Contributions to the genetics, taxonomy, and ecology of Drosophila pseudoobscura and its relatives. Carnegie Inst Wash Publ 554:1–183
Dowling DK, Nowostawski A, Arnqvist G (2007) Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle: implications for sperm competition theory? J Evol Biol 20:358–368
Dunn A, Andrews T, Ingrey H, Riley J, Wedell N (2006) Strategic sperm allocation under parasitic sex ratio distortion. Biol Lett 2:78–80
Evans JP, Zane L, Francescato S, Pilastro A (2003) Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360–363
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
Fishman L, Willis JH (2005) A novel meiotic drive locus almost completely distorts segregation in Mimulus (monkeyflower) hybrids. Genetics 169:347–353
Fishman L, Willis JH (2006) A cytonuclear incompatibility causes anther sterility in Mimulus hybrids. Evolution 60:1372–1381
Froman DP, Pizarri T, Feltmann AJ, Castillo-Juares H, Birkhead TR (2002) Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc R Soc B 269:607–612
Fry CL, Wilkinson GS (2004) Sperm survival in female stalk-eyed flies depends on seminal fluid and meiotic drive. Evolution 58:1622–1626
Gemmel NJ, Sin FYT (2002) Mitochondrial mutations may drive Y chromosome evolution. BioEssays 24:275–279
González-Sánchez M, Chiavarino M, Jiménez G, Rosato M, Puertas MJ (2004) The parasitic effects of rye B chromosomes might be beneficial in the long run. Cytogenet Genome Res 106:386–393
Hackstein JH, Hochstenbach R, Hauschteck-Jungen E, Beukeboom LW (1996) Is the Y chromosome of Drosophila an evolved supernumary chromosome? BioEssays 18:317–323
Haig D, Bergstrom CT (1995) Multiple mating, sperm competition and meiotic drive. J Evol Biol 8:265–282
Hanson MR, Bentolila S (2004) Interactions of mitochondrial and nuclear genes that affect male gametophyte development. Plant Cell 16:s154–s169
Hartl DL, Hiraizumi Y, Crow JF (1967) Evidence for sperm dysfunction as the mechanism of segregation distortion in Drosophila melanogaster. Genetics 58:2240–2245
Hoffmann AA, Turelli M (1988) Unidirectional incompatibility in Drosophila simulans: Inheritance, geographic variation and fitness effects. Genetics 119:435–444
Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatability in Drosophila simulans. Genetics 126:933–948
Hosken DJ, Garner TWJ, Tregenza T, Wedell N, Ward PI (2003) Superior sperm competitors sire higher quality young. Proc R Soc B 270:1933–1938
Hosken DJ, Garner TWJ, Ward PI (2001) Sexual conflict selects for male and female reproductive characters. Curr Biol 11:489–493
Hosken DJ, Stockley P (2003) Benefits of polyandry: a life history perspective. Evol Biol 33:173–194
Jaenike J (1996) Sex-ratio meiotic drive in the Drosophila quinaria group. Am Nat 148:237–254
Jaenike J (1999) Y-chromosome polymorphism in Drosophila. Evolution 53:164–174
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 175:21–64
Jeong G, Stouthamer R (2006) Influence of postzygotic reproductive isolation on the interspecific transmission of the paternal sex ratio chromosome in Trichogramma. Entom Exp et Appl 120:33–40
Jiggins FM, Randerson JP, Hurst GDD, Majerus MEN (2002) How can sex ratio distorters reach extreme prevalences? Male-killing Wolbachia are not suppressed and have near-perfect vertical transmission efficiency in Acraea encedon. Evolution 56:2290–2295
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
Jones RN (1995) B chromosomes in plants: escapees from the A chromosome genome. New Phytol 131:411–434
Jones RN, Rees H (1982) B chromosomes. Academic Press, London
Kaul MLH (1988) Male sterility in higher plants. Springer-Verlag, Berlin
Kelly A, Hatcher MJ, Evans L, Dunn A (2001) Mate choice and mate guarding under the influence of a vertically transmitted, parasitic sex ratio distorter. Anim Behav 61:763–770
Kimura M, Kayano H (1961) The maintenance of supernumerary chromosomes in wild populations of Lilium callosum by preferential segregation. Genetics 46:1699–1712
Kleene KC (2005) Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. Dev Biol 277:16–26
Kleene KC, Cataldo L, Mastrangelo M-A, Tagne JB (2003) Alternative patterns of transcriptions and translation of the ribosomal protein L32 mRNA in somatic and spermatogenic cells in mice. Exp Cell Res 291:101–110
Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiostisi SN (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60:87–96
Lande R, Wilkinson GS (1999) Models of sex-ratio meiotic drive and sexual selection in stalk-eyed flies. Genet Res 74:245–253
Lane N (2005) Power, sex, suicide: mitochondria and the meaning of life. Oxford University Press, Oxford
LeGrand E (2001) Genetic conflict and apoptosis. Persp Biol Med 44:509–521
Lenington S (1983) Social preferences for partners carrying ‘good genes’ in wild house mice. Anim Behav 31:325–333
Lenington S (1991) The t-complex: a story of genes, behavior, and populations. Adv Study Behav 20:51–86
Lewis D (1941) Male sterility in natural populations of hermaphrodite plants: the equilibrium between females and hermaphrodites to be expected with different types of inheritance. New Phytol 40:56–63
Lopez-Leon MD, Cabrero J, Camacho JPM (1996) Negatively assortitative gamete fertilization for supernumerary heterochromatin in two grasshopper species. Heredity 76:651–657
Lopez-Leon MD, Martinalganza A, Pardo MC, Cabrero J, Camacho JPM (1995) Temporal frequency stability and absence of effects on mating behavior for an autosomal supernumerary segment in 2 natural populations of the grasshopper Eyprepocnemis plorans. Genome 38:320–324
Lyttle TW (1991) Segregation distorters. Ann Rev Genet 25:511–557
Martin S, Arana P, Henriques-Gil N (1996) The effect of B chromosomes on mating success of the grasshopper Eyprepocnemis plorans. Genetica 97:197–203
McKee B, Lindsley DL (1987) Inseparability of X-heterochromatic functions responsible for X:Y pairing, meiotic drive, and male fertility in Drosophila melanogaster. Genetics 116:399–407
Moreau J, Bertin A, Caubet Y, Rigaud T (2001) Sexual selection in an isopod with Wolbachia-induced sex reversal: males prefer real females. J Evol Biol 14:388–394
Morrow EH, Gage MJG (2001) Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87:356–362
Nasuda S, Friebe B, Gill BS (1998) Gametocidal genes induce chromosome breakage in the interphase prior to the first mitotic cell division of the male gametophyte in wheat. Genetics 149:1115–1124
Newcomer SD, Zeh JA, Zeh DW (1999) Genetic benefits enhance the reproductive success of polyandrous females. Proc Natl Acad Sci USA 96:10236–10241
Nichols RA, Butlin RK (1989) Does selection work in finite populations? J Evol Biol 2:299–313
Nur U (1966) The effect of supernumerary chromosomes on the development of mealy bugs. Genetics 54:1239–1249
Orr HA, Irving S (2005) Segregation distortion in hybrids between the Bogota and USA subspecies of Drosophila pseudoobscura. Genetics 169:671–682
Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Moller AP (eds) Sperm Competition and Sexual Selection. Academic Press, New York
Peirce EJ, Breed WG (2001) A comparative study of sperm production in two species of Australian arid zone rodents (Pseudomys australis, Notomys alexis) with marked differences in testis size. Reproduction 1221:239–247
Policansky D, Ellison J (1970) “Sex ratio” in Drosophila pseudoobscura: spermiogenic failure. Science 169:888–889
Pomiankowski A, Hurst LD (1999) Driving sexual preference. Trends Ecol Evol 14:425–426
Puertas MJ, Carmona R (1976) Greater ability of pollen tube growth in rye plants with 2B chromosomes. Theor Appl Genet 47:41–43
Quillet MC, Madjidian N, Griveau Y, Serieys H, Tersac M, Lorieux M, Berville A (1995) Mapping genetic factors controlling pollen viability in an interspecific cross in Helianthus sect. Helianthus. Theor Appl Genet 91:1195–1202
Rajendra TK, Prasanth KV, Lakhotia SC (2001) Male sterility associated with overexpression of the noncoding hsr omega gene in cyst cells of testis of Drosophila melanogaster. J Genet 80:97–110
Randerson JP, Jiggins FM, Hurst LD (2000) Male killing can select for male mate choice: a novel solution to the paradox of the lek. Proc R Soc B 267:867–874
Reinhold K, Engqvist L, Misof B, Kurtz J (1999) Meiotic drive and evolution of female choice. Proc R Soc B 266:1341–1345
Remis MI, Vilardi JC (2004) Mitotically unstable B chromosome polymorphism in the grasshopper Dichroplus elongatus. Genome Res 106:359–364
Rick CM (1966) Abortion of male and female gametes in the tomato determined by allelic interaction. Genetics 53:85–96
Rigaud T, Moreau J (2004) A cost of Wolbachia-induced sex reversal and female-biased sex ratios: decrease in female fertility after sperm depletion in a terrestrial isopod. Proc R Soc B 271:1941–1946
Rosetti N, Vilardi JC, Remis MI (2007) Effects of B chromosomes and supernumerary segments on morphometric traits and adult fitness components in the grasshopper, Dichroplus elongatus (Acrididae). J Evol Biol 20:249–259
Saur MJ, Wade MJ (2003) A synthetic view of the theory of gynodioecy. Am Nat 161:837–851
Schärer L, Ladurner P, Rieger RM (2004) Bigger testes do work more: experimental evidence that testis size reflects testicular cell proliferation activity in the marine invertebrate, the free-living flatworm Macrostomum sp. Behav Ecol Sociobiol 56:420–425
Schimenti J (2000) Segregation distortion of mouse t haplotypes: the molecular basis emerges. Trends Genet 16:240–243
Schnable PS, Wise RP (1998) The molecular basis of cytoplasmic male sterility and fertility restoration. Trends Plant Sci 3:175–180
Silver LM (1993) The peculiar journey of a selfish chromosome: mouse t haplotypes and meiotic drive. Trends Genet 9:250–254
Simmons LW (2001) Sperm competition and its evolutionary consequences in insects. Princeton University Press, Princeton
Singh SR, Singh BN, Hoenigsberg HF (2002) Female remating, sperm competition and sexual selection in Drosophila. Genet Mol Res 1:178–215
Snook RR, Cleland SY, Wolfner MF, Karr TL (2000) Offsetting effects of Wolbachia infection and heat shock on sperm production in Drososphila simulans: analyses of fecundity, fertility and accessory gland proteins. Genetics 155:167–178
St John JC, Jokhi RP, Barratt CLR (2005) The impact of mitochondrial genetics on male infertility. Int J Androl 28:65–73
Stockley P, Gage MJG, Parker GA, Moller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954
Sullivan J, Jaenike J (2006) Male-killing Wolbachia and male mate choice: a test with Drosophila innubila. Evol Ecol Res 8:91–102
Summers K, da Silva J, Farwell M (2002) Intragenomic conflict and cancer. Med Hypotheses 59:170–179
Tao Y, Hartl DL, Laurie CC (2001) Sex-ratio segregation distortion associated with reproductive isolation in Drosophila. Proc Natl Acad Sci USA 98:13183–13188
Taylor DR, Ingvarsson PK (2003) Common features of segregation distortion in plants and animals. Genetica 117:27–35
Taylor DR, Jaenike J (2002) Sperm competition and the dynamics of X chromosome drive: stability and extinction. Genetics 160:1721–1751
Taylor DR, Saur MJ, Adams E (1999) Pollen performance and sex-ratio evolution in a dioecious plant. Evolution 53:1028–1036
Torgerson DG, Singh RS (2000) Sex-linked mammalian sperm proteins evolve faster than autosomal ones. Mol Biol Evol 20:1705–1709
Tregenza T, Wedell N (2000) Genetic incompatibility, mate choice and patterns of parentage: invited review. Mol Ecol 9:1013–1027
Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415:71–73
Vala F, Egas M, Breeuwer JAJ, Sabelis MW (2004) Wolbachia affects oviposition and mating behaviour of its spider mite host. J Evol Biol 17:692–700
Wade MJ, Chang NW (1995) Increased male fertility in Tribolium confusum beetles after infection with the intracellular parasite Wolbachia. Nature 373:72–74
Wang PJ, McCarrey JR, Yang F, Page DC (2001) An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27:422–426
Ward PI (2000) Sperm length is heritable and sex-linked in the yellow dung fly (Scatophaga stercoraria). J Zool 251:349–353
Wilkinson GS, Fry CL (2001) Meiotic drive alters sperm competitive ability in stalk-eyed flies. Proc R Soc B 268:2559–2564
Wilkinson GS, Johns PM, Kelleher ES, Muscedere ML, Lorsong A (2006) Fitness effects of X chromosome drive in the stalk-eyed fly, Cyrtodiopsis dalmanni. J Evol Biol 19:1851–1860
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
Wilkinson GS, Sanchez MI (2001) Sperm development, age and sex chromosome meiotic drive in the stalk-eyed fly, Cyrtodiopsis whitei. Heredity 87:17–24
Williams J, Lenington S (1993) Environmental and genetic factors affecting preferences of female house mice (Mus domesticus) for males that differ in t-complex genotype. Behav Genet 23:51–58
Wood RJ, Newton ME (1991) Sex-ratio distortion caused by meiotic drive in mosquitoes. Am Nat 137:379–391
Wu C-I (1983a) Virility deficiency and the sex-ratio trait in Drososphila pseudoobscura. I. Sperm displacement and sexual selection. Genetics 105:651–662
Wu C-I (1983b) Virility deficiency and the sex-ratio trait in Drososphila pseudoobscura. II. Multiple mating and overall virility selection. Genetics 105:663–679
Zeh JA, Zeh DW (1996) The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc R Soc B 263:1711–1717
Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc B 264:69–75
Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051–1063
Zendman AJM, Ruiter DJ, van Muijen GNP (2003) Cancer/testis-associated genes: identification, expression profile, and putative function. J Cell Physiol 194:272–288
Zollner S, Wen X, Hanchard NA, Herbert MA, Ober C, Pritchard JK (2004) Evidence for extensive transmission distortion in the human genome. Am J Hum Genet 74:62–72
Acknowledgements
We would like to thank Trevor Pitcher and Herman Mays for kindly inviting us to participate in ‘The evolutionary ecology of genetic quality symposium’, and David Hosken and the two anonymous referees for insightful comments on the MS. This work was supported by a NERC grant and funds from the European Science Foundation.
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Price, T.A.R., Wedell, N. Selfish genetic elements and sexual selection: their impact on male fertility. Genetica 132, 295–307 (2008). https://doi.org/10.1007/s10709-007-9173-2
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DOI: https://doi.org/10.1007/s10709-007-9173-2