Evolutionary Biology

, Volume 38, Issue 2, pp 115–123 | Cite as

Using Parthenogenetic Lineages to Identify Advantages of Sex

Synthesis Paper

Abstract

The overwhelming predominance of sexual reproduction in nature is surprising given that sex is expected to confer profound costs in terms of production of males and the breakup of beneficial allele combinations. Recognition of these theoretical costs was the inspiration for a large body of empirical research—typically focused on comparing sexual and asexual organisms, lineages, or genomes—dedicated to identifying the advantages and maintenance of sex in natural populations. Despite these efforts, why sex is so common remains unclear. Here, we argue that we can generate general insights into the advantages of sex by taking advantage of parthenogenetic taxa that differ in such characteristics as meiotic versus mitotic offspring production, ploidy level, and single versus multiple and hybrid versus non-hybrid origin. We begin by evaluating benefits that sex can confer via its effects on genetic linkage, diversity, and heterozygosity and outline how the three classes of benefits make different predictions for which type of parthenogenetic lineage would be favored over others. Next, we describe the type of parthenogenetic model system (if any) suitable for testing whether the hypothesized benefit might contribute to the maintenance of sex in natural populations, and suggest groups of organisms that fit the specifications. We conclude by discussing how empirical estimates of characteristics such as time since derivation and number of independent origins of asexual lineages from sexual ancestors, ploidy levels, and patterns of molecular evolution from representatives of these groups can be used to better understand which mechanisms maintain sex in natural populations.

Keywords

Asexuality Parthenogenesis Meiosis Sexual reproduction 

Notes

Acknowledgments

M. Neiman acknowledges funding from the Carver Trust and the University of Iowa, and T. Schwander from the Netherlands Organisation for Scientific Research.

Supplementary material

11692_2011_9113_MOESM1_ESM.pdf (42 kb)
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References

  1. Archetti, M. (2010). Complementation, genetic conflict, and the evolution of sex and recombination. Journal of Heredity, 101, S21–S33.PubMedCrossRefGoogle Scholar
  2. Barton, N. H., & Otto, S. P. (2005). Evolution of recombination due to random drift. Genetics, 169, 2353–2370.PubMedCrossRefGoogle Scholar
  3. Bell, G. (1982). The masterpiece of nature. London: Croon Helm.Google Scholar
  4. Beukeboom, L. W., Weinzierl, R. P. K., Reed, M., & Michiels, N. K. (1996). Distribution and origin of chromosomal races in the freshwater planarian Duglesia polychroa (Turbellaria: Tricladida). Hereditas, 125, 7–15.Google Scholar
  5. Bierzychudek, P. (1985). Patterns in plant parthenogenesis. Experientia, 41, 1255–1264.CrossRefGoogle Scholar
  6. Birky, C. W., & Walsh, J. B. (1988). Effects of linkage on rates of molecular evolution. Proceedings of the National Academy of Sciences of the United States of America, 85, 6414–6418.PubMedCrossRefGoogle Scholar
  7. Black, F. L., & Hedrick, P. W. (1997). Strong balancing selection at HLA loci: Evidence from segregation in South Amerindian families. Proceedings of the National Academy of Sciences of the United States of America, 94, 12452–12456.PubMedCrossRefGoogle Scholar
  8. Browne, R. A. (1992). Population genetics and ecology of Artemia: Insights into parthenogenetic reproduction. Trends in Ecology & Evolution, 7, 232–237.CrossRefGoogle Scholar
  9. Burt, A. (2000). Perspective: Sex, recombination, and the efficacy of selection—Was Weismann right? Evolution, 54, 337–351.PubMedGoogle Scholar
  10. Carrington, M., Nelson, G. W., Martin, M. P., Kissner, T., Vlahov, D., et al. (1999). HLA and HIV-1: Heterozygote advantage and B*35-Cw*04 disadvantage. Science, 283, 1748–1752.PubMedCrossRefGoogle Scholar
  11. Charlesworth, D., Morgan, M. T., & Charlesworth, B. (1993). Mutation accumulation in finite outbreeding and inbreeding populations. Genetical Research, 61, 39–56.CrossRefGoogle Scholar
  12. Christensen, B. (1961). Studies on cyto-taxonomy and reproduction in Enchytraeidae- with notes on parthenogenesis and polyploidy in the animal kingdom. Hereditas, 47, 387.CrossRefGoogle Scholar
  13. Christensen, B., Hvilsom, M. M., & Pedersen, B. V. (1989). On the origin of clonal diversity in parthenogenetic Fridericia striata (Enchytraeidae, Oligochaeta). Hereditas, 110, 89–91.CrossRefGoogle Scholar
  14. Coltman, D. W., Pilkington, J. G., Smith, J. A., & Pemberton, J. M. (1999). Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution, 53, 1259–1267.CrossRefGoogle Scholar
  15. Crow, J. F., & Kimura, M. (1970). An introduction to population genetics theory. New York: Harper and Row.Google Scholar
  16. D’Souza, T. G., Storhas, M., Schulenburg, H., Beukeboom, L. W., & Michiels, N. K. (2004). Occasional sex in an ‘asexual’ polyploid hermaphrodite. Proceedings of the Royal Society of London B, 271, 1001–1007.CrossRefGoogle Scholar
  17. de Visser, J., & Elena, S. F. (2007). The evolution of sex: Empirical insights into the roles of epistasis and drift. Nature Reviews Genetics, 8, 139–149.PubMedCrossRefGoogle Scholar
  18. Decaestecker, E., Gaba, S., Raeymaekers, J. A. M., Stoks, R., Van Kerckhoven, L., Ebert, D., et al. (2007). Host-parasite ‘Red Queen’ dynamics archived in pond sediment. Nature, 450, 870–873.PubMedCrossRefGoogle Scholar
  19. Felsenstein, J. (1974). The evolutionary advantages of recombination. Genetics, 78, 737–756.PubMedGoogle Scholar
  20. Felsenstein, J., & Yokoyama, S. (1976). The evolutionary advantage of recombination. II. Individual selection for recombination. Genetics, 83, 845–859.PubMedGoogle Scholar
  21. Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Clarendon Press.Google Scholar
  22. Fontaneto, D., Herniou, E. A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C., et al. (2007). Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5, 914–921.CrossRefGoogle Scholar
  23. Green, R. F., & Noakes, D. L. G. (1995). Is a little of bit of sex as good as a lot? Journal of Theoretical Biology, 174, 87–96.CrossRefGoogle Scholar
  24. Haccou, P., & Schneider, M. V. (2004). Modes of reproduction and the accumulation of deleterious mutations with multiplicative fitness effects. Genetics, 166, 1093–1104.PubMedCrossRefGoogle Scholar
  25. Hadany, L., & Comeron, J. M. (2008). Why are sex and recombination so common? Annals of the New York Academy of Sciences, 1133, 26–43.PubMedCrossRefGoogle Scholar
  26. Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science, 218, 384–387.PubMedCrossRefGoogle Scholar
  27. Hastings, A., & Harrison, S. (1994). Metapopulation dynamics and genetics. Annual Review of Ecology and Systematics, 25, 167–188.CrossRefGoogle Scholar
  28. Hedrick, P. W., & Thomsom, G. (1983). Evidence for balancing selection at HLA. Genetics, 104, 449–456.PubMedGoogle Scholar
  29. Hill, W. G., & Robertson, A. (1966). Effect of linkage on limits to artificial selection. Genetical Research, 8, 269–294.PubMedCrossRefGoogle Scholar
  30. Johnson, S. G., & Howard, R. S. (2007). Contrasting patterns of synonymous and nonsynonymous sequence evolution in asexual and sexual freshwater snail lineages. Evolution, 61, 2728–2735.PubMedCrossRefGoogle Scholar
  31. Jokela, J., Dybdahl, M. F., & Lively, C. M. (2009). The maintenance of sex, clonal dynamics, and host-parasite coevolution in a mixed population of sexual and asexual snails. American Naturalist, 174, S43–S53.Google Scholar
  32. Judson, O. P., & Normark, B. B. (1996). Ancient asexual scandals. Trends in Ecology & Evolution, 11, 41–46.CrossRefGoogle Scholar
  33. Keightley, P. D., & Otto, S. P. (2006). Interference among deleterious mutations favours sex and recombination in finite populations. Nature, 443, 89–92.PubMedCrossRefGoogle Scholar
  34. Kondrashov, A. S. (1993). Classification of hypotheses on the advantage of amphimixis. Journal of Heredity, 84, 372–387.PubMedGoogle Scholar
  35. Kramer, M. G., & Templeton, A. R. (2001). Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum. Evolution, 55, 748–761.PubMedCrossRefGoogle Scholar
  36. Lively, C. M. (2010). A review of Red Queen models for the persistence of obligate sexual reproduction. Journal of Heredity, 101, S13–S20.PubMedCrossRefGoogle Scholar
  37. Lundmark, M. (2006). Polyploidization, hybridization and geographical parthenogenesis. Trends in Ecology & Evolution, 21, 9.CrossRefGoogle Scholar
  38. Lynch, M., Burger, R., Butcher, D., & Gabriel, W. (1993). The mutational meltdown in asexual populations. Journal of Heredity, 84, 339–344.PubMedGoogle Scholar
  39. Maynard Smith, J. (1971). The origin and maintenance of sex. In G. C. Williams (Ed.), Group selection (pp. 164–175). Chicago: Aldine-Atherton.Google Scholar
  40. Maynard Smith, J. (1978). The evolution of sex. New York: Cambridge University Press.Google Scholar
  41. Morris, J. A., & Harrison, L. M. (2009). Hypothesis: Increased male mortality caused by infection is due to a decrease in heterozygous loci as a result of a single X chromosome. Medical Hypotheses, 72, 322–324.PubMedCrossRefGoogle Scholar
  42. Muller, H. J. (1964). The relation of recombination to mutational advance. Mutation Research, 1, 2–9.Google Scholar
  43. Müller, H. J. (1932). Some genetic aspects of sex. American Naturalist, 66, 118–138.CrossRefGoogle Scholar
  44. Neiman, M., Hehman, G., Miller, J. T., Logsdon, J. M., & Taylor, D. R. (2010). Accelerated mutation accumulation in asexual lineages of a freshwater snail. Molecular Biology and Evolution, 27, 954–963.PubMedCrossRefGoogle Scholar
  45. Neiman, M., & Koskella, B. (2009). Sex and the Red Queen. In I. Schön, K. Martens, & P. van Dijk (Eds.), Lost sex (pp. 133–159). Amsterdam: Springer.CrossRefGoogle Scholar
  46. Neiman, M., Meirmans, S., & Meirmans, P. G. (2009). What can asexual lineage age tell us about the maintenance of sex? Annals of the New York Academy of Sciences, 1168, 185–200.PubMedCrossRefGoogle Scholar
  47. Neiman, M., & Taylor, D. R. (2009). The causes of mutation accumulation in mitochondrial genomes. Proceedings of the Royal Society B, 276, 1201–1209.PubMedCrossRefGoogle Scholar
  48. Normark, B. B., & Moran, N. A. (2000). Testing for the accumulation of deleterious mutations in asexual eukaryote genomes using molecular sequences. Journal of Natural History, 34, 1719–1729.CrossRefGoogle Scholar
  49. Ohta, T., & Kimura, M. (1971). On the constancy of the evolutionary rate of cistrons. Journal of Molecular Evolution, 1, 18–25.CrossRefGoogle Scholar
  50. Ortego, J., Aparicio, J. M., Calabuig, G., & Cordero, P. J. (2007). Risk of ectoparasitism and genetic diversity in a wild lesser kestrel population. Molecular Ecology, 16, 3712–3720.PubMedCrossRefGoogle Scholar
  51. Otto, S. P. (2009). The evolutionary enigma of sex. American Naturalist, 174, S1–S14.PubMedCrossRefGoogle Scholar
  52. Otto, S. P., & Barton, N. H. (1997). The evolution of recombination: removing the limits to natural selection. Evolution, 147, 879–906.Google Scholar
  53. Otto, S. P., & Whitton, J. (2000). Polyploid incidence and evolution. Annual Review of Genetics, 34, 401–437.PubMedCrossRefGoogle Scholar
  54. Paland, S., & Lynch, M. (2006). Transitions to asexuality result in excess amino acid substitutions. Science, 311, 990–992.PubMedCrossRefGoogle Scholar
  55. Pamilo, F., Nei, M., & Li, W. H. (1987). Accumulation of mutations in sexual and asexual populations. Genetical Research, 49, 135–146.PubMedCrossRefGoogle Scholar
  56. Paquin, C. E., & Adams, J. (1983). Frequency of fixation of adaptive mutations is higher in diploid than in haploid populations. Nature, 302, 495–500.PubMedCrossRefGoogle Scholar
  57. Pearcy, M., Hardy, O., & Aron, S. (2006). Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity, 96, 377–382.PubMedCrossRefGoogle Scholar
  58. Pongratz, N., Storhas, M., Carranza, S., & Michiels, N. K. (2003). Phylogeography of competing sexual and parthenogenetic forms of a freshwater flatworm: Patterns and explanations. BMC Evolutionary Biology, 3, 23.PubMedCrossRefGoogle Scholar
  59. Rice, W. R. (2002). Experimental tests of the adaptive significance of sexual recombination. Nature Reviews Genetics, 3, 241–251.PubMedCrossRefGoogle Scholar
  60. Richards, A. J. (1997). Plant breeding systems. Cheltenham, UK: Stanley Thornes.Google Scholar
  61. Robertson, A. (1961). Inbreeding in artificial selection programmes. Genetical Research, 2, 189.CrossRefGoogle Scholar
  62. Roze, D., & Barton, N. H. (2006). The Hill-Robertson effect and the evolution of recombination. Genetics, 173, 1793–1811.PubMedCrossRefGoogle Scholar
  63. Schwander, T., Vuilleumier, S., Dubman, J., & Crespi, B. J. (2010). Positive feedback in the transition from sexual reproduction to parthenogenesis. Proceedings of the Royal Society B, 277, 1435–1442.PubMedCrossRefGoogle Scholar
  64. Spurgin, L. G., & Richardson, D. S. (2010). How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proceedings of the Royal Society of London B, 277, 979–988.CrossRefGoogle Scholar
  65. Stenberg, P., & Saura, A. (2009). Cytology of asexual animals. In I. Schön, K. Martens, & P. van Dijk (Eds.), Lost sex. The evolutionary biology of Parthenogenesis (pp. 63–74). Amsterdam: Springer.CrossRefGoogle Scholar
  66. Suomalainen, E., Saura, A., & Lokki, J. (1987). Cytology and evolution in parthenogenesis. Boca Raton, FL: CRC Press.Google Scholar
  67. Suomaleinen, E. (1950). Parthenogenesis in animals. Advances in Genetics, 3, 193–253.CrossRefGoogle Scholar
  68. Tagg, N., Innes, D. J., & Doncaster, C. P. (2005). Outcomes of reciprocal invasions between genetically diverse and genetically uniform populations of Daphnia obtusa (Kurz). Oecologia, 143, 527–536.PubMedCrossRefGoogle Scholar
  69. Templeton, A. R. (1982). The prophecies of parthenogenesis. In H. Dingle & J. P. Hegmann (Eds.), Evolution and genetics of life histories (pp. 75–101). New York: Springer.Google Scholar
  70. Thursz, M. R., Thomas, H. C., Greenwood, B. M., & Hill, A. V. S. (1997). Heterozygote advantage for HLA class-II type in hepatitis B virus infection. Nature Genetics, 17, 11–12.PubMedCrossRefGoogle Scholar
  71. Wade, M. J., & Goodnight, C. J. (1998). Perspective: The theories of Fisher and Wright in the context of metapopulations: When nature does many small experiments. Evolution, 52, 1537–1553.CrossRefGoogle Scholar
  72. Williams, G. C. (1971). Introduction. In G. C. Williams (Ed.), Group selection (pp. 1–15). Chicago: Aldine-Atherton.Google Scholar
  73. Williams, G. C. (1975). Sex and evolution. Princeton, NJ: Princeton University Press.Google Scholar
  74. Williams, G. C., & Mitton, J. B. (1973). Why reproduce sexually? Journal of Theoretical Biology, 39, 545–554.PubMedCrossRefGoogle Scholar
  75. Woelfing, B., Traulsen, A., Milinksi, M., & Boehm, T. (2009). Does intra-individual major histocompatibility complex diversity keep a golden mean? Philosophical Transactions of the Royal Society of London Series B, 364, 117–128.PubMedCrossRefGoogle Scholar
  76. Wolinska, J., & Lively, C. M. (2008). The cost of males in Daphnia pulex. Oikos, 117, 1637–1646.CrossRefGoogle Scholar
  77. Wright, S. (1931). Evolution in Mendelian populations. Genetics, 16, 97–159.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of BiologyUniversity of IowaIowa CityUSA
  2. 2.Evolutionary Genetics, Center for Ecological and Evolutionary StudiesUniversity of GroningenGroningenThe Netherlands

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