Abstract
Important questions remain about the long-term survival and adaptive significance of eukaryotic asexual lineages. Numerous papers dealing with sex advantages still continued to compare parthenogenetic populations versus sexual populations arguing that sex demonstrates a better fitness. Because asexual lineages do not possess any recombination mechanisms favoring rapid changes in the face of severe environmental conditions, they should be considered as an evolutionary dead-end. Nevertheless, reviewing literature dealing with asexual reproduction, it is possible to draw three stimulating conclusions. (1) Asexual reproduction in eukaryotes considerably differs from prokaryotes which experience recombination but neither meiosis nor syngamy. Recombination and meiosis would be a driving force for sexual reproduction. Eukaryotes should therefore be considered as a continuum of sexual organisms that are more or less capable (and sometimes incapable) of sexual reproduction. (2) Rather than revealing ancestral eukaryotic forms, most known lineages of asexual eukaryotes have lost sex due to a genomic conflict affecting their sexual capacity. Thus, it could be argued that hybridization is a major cause of their asexuality. Asexuality may have evolved as a reproductive mechanism reducing conflict within organisms. (3) It could be proposed that, rather than being generalists, parthenogenetic hybrid lineages could be favored when exploiting peculiar restricted ecological niches, following the “frozen niche variation” model. Although hybrid events may result in sex loss, probably caused by genomic conflict, asexual hybrids could display new original adaptive traits, and the rapid colonization of environments through clonal reproduction could favor their long-term survival, leading to evolutionary changes and hybrid speciation. Examination of the evolutionary history of asexual lineages reveals that evolutionary processes act through transitional stages in which even very small temporary benefits may be enough to counter the expected selective disadvantages.
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References
Agrawal, A. F. (2009). Differences between selection on sex versus recombination in red queen models with diploid hosts. Evolution, 63, 2131–2141.
Angers, B., & Schlosser, I. J. (2007). The origin of Phoxinus eos-neogaeus unisexual hybrids. Molecular Ecology, 16, 4562–4571.
Arkhipova, I., & Meselson, M. (2004). Deleterious transposable elements and the extinction of asexuals. BioEssays, 27, 76–85.
Arnold, M. L. (1996). Natural hybridization and evolution. New York: Oxford University Press.
Baker, H. G., & Stebbins, G. I. (1965). The genetics of colonizing species. New York: Academic Press.
Barraclough, T. G., Birky, C. W., Jr, & Burt, A. (2003). Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.
Barton, N. H., & Charlesworth, B. (1998). Why sex and recombination? Science, 281, 1986–1990.
Bell, G. (1993). The sexual nature of eukaryote genomes. Journal of Heredity, 84, 351–359.
Bernstein, H., Byerly, H. C., Hopf, F. A., & Michod, R. E. (1984). Origin of sex. Journal of Theoretical of Biology, 110, 323–351.
Beukeboom, L., & Vrijenhoek, R. C. (1998). Evolutionary genetics and ecology of sperm-dependent parthenogenesis. Journal of Evolutionary Biology, 11, 755–782.
Birky, W. C., Jr. (2004). Bdelloid rotifer revisited. Proceedings of the National Academy of Sciences USA, 101, 2651–2652.
Bjork, A., & Pitnik, S. (2006). Intensity of sexual selection along the anisogamy-isogamy continuum. Nature, 441, 742–745.
Brown, S. G., Kwan, S., & Shero, S. (1995). The parasitic theory of sexual reproduction, parasitism in unisexual and bisexual geckos. Proceedings of the Royal Society of London B, 260, 317–320.
Bruvo, R., Adolfsson, S., Symonova, R., Lamatsch, D. K., Schön, I., Jokela, J., et al. (2011). Few parasites, and no evidence for Wolbachia infections in a freshwater ostracod inhabiting temporary ponds. Biological Journal of the Linnaean Society of London, 102, 208–216.
Butlin, R. (2002). The costs and benefits of sex, new insights from old asexual lineages. Nature Reviews of Genetics, 3, 311–317.
Butlin, R. K., & Griffiths, H. I. (1993). Ageing without sex? Nature, 364, 680.
Carman, J. G. (1997). Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biological Journal of the Linnaean Society of London, 61, 51–94.
Carman, J. G. (2007). Do duplicate genes cause apomixes? In E. Hörandl, U. Grossniklaus, P. J. van Dijk, & T. F. Sharbel (Eds.), Apomixis, evolution, mechanisms and perspectives (pp. 63–91). Liechtenstein: Gantner Rugell.
Cavalier-Smith, T. (2002). Origins of the machinery of recombination and sex. Heredity, 8, 125–141.
Chaplin, J. A., Havel, J. E., & Hebert, P. D. N. (1994). Sex and ostracods. Trends in Ecology & Evolution, 9, 435–439.
Christin, P. A., Edwards, E. J., Besnard, G., Boxall, S. F., Gregory, R., Kellogg, E. A., et al. (2012). Adaptive evolution of C4 Photosynthesis through recurrent lateral gene transfer. Current Biology, 22, 445–449.
Clay, K., & Kover, P. X. (1996). The Red Queen hypothesis and plant/pathogen interactions. Annuals Reviews of Phytopathology, 34, 29–50.
Cooper, T. F. (2007). Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biology, 59, e225.
Coyne, J. A., & Orr, H. A. (1993). Further evidence against meiotic-drive models of hybrid sterility. Evolution, 47, 685–687.
Crews, D. (2012). The (bi)sexual brain. EMBO Reports, 13, 779–784.
Crews, D., & Bull, J. J. (2009). Mode and tempo in environmental sex determination in vertebrates. Seminar Cell Development Biology, 20, 251–255.
Crews, D., Grassman, M., & Lindzey, J. (1986). Behavioral facilitation of reproduction in sexual and unisexual whiptail lizards. Proceedings of the National Academy of Sciences USA, 83, 9547–9550.
Cullum, A. (2000). Phenotypic variability of physiological traits in populations of sexual and asexual whiptail lizards (genus Cnemidophorus). Evolutionary Ecology Research, 2, 841–855.
Czárán, T. L., & Hoesktra, R. F. (2004). Evolution of sexual asymmetry. BMC Evolutionary Biology, 4, 34.
de Queiroz, K. (2005). Ernst Mayr and the modern concept of species. Proceedings of the National Academy of Sciences USA, 102, 6600–6607.
de Visser, J. A. G. M., & Elena, S. F. (2007). The evolution of sex: Empirical insights into the roles of epistasis and drift. Nature Reviews of Genetics, 8, 139–149.
Domes, K., Norton, R. A., Maraun, M., & Scheu, S. (2007). Revolution of sexuality breaks Dollo’s law. Proceedings of the National Academy of Sciences USA, 104, 7139–7144.
Dujardin, M., & Hanna, W. W. (1989). Developing apomictic pearl millet characterization of a BC3 plant. Journal of Genetic Breeding, 43, 145–151.
Dunthorn, M., & Katz, L. (2010). Secretive ciliates and putative asexuality in microbial eukaryotes. Trends in Microbiology, 18, 183–188.
Dyer, P. S., & Paoletti, M. (2005). Reproduction in Aspergillus fumigatus, sexuality in a supposedly asexual species? Medical Mycology Supplement, 43, S7–S14.
Egel, R. (2000). Fission yeast on the brink of meiosis. BioEssays, 22, 854–860.
Felsenstein, J. (1974). The evolutionary advantage of recombination. Genetics, 78, 737–756.
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, e87.
Genner, M. J., & Turner, G. F. (2012). Ancient hybridization and phenotypic novelty within Lake Malawi’s Cichlid fish radiation. Molecular Biology and Evolution, 29, 195–206.
Ghiselli, F., Milani, L., Scali, V., & Passamonti, M. (2007). The Leptynia hispanica species complex (Insecta Phasmida), polyploidy, parthenogenesis, hybridization and more. Molecular Ecology, 16, 4256–4268.
Gilbert, C., Hernandez, S. S., Flores-Benabib, J., Smith, E. N., & Feschotte, C. (2012). Rampant horizontal transfer of SPIN transposons in Squamate Reptiles. Molecular Biology and Evolution, 29, 503–515.
Goddard, M. R., Godfray, H. C. J., & Burt, A. (2005). Sex increases the efficacy of natural selection in experimental yeast populations. Nature, 434, 636–640.
Goldberg, E. E., & Igic, B. (2008). On phylogenetic tests of irreversible evolution. Evolution, 62, 2727–2741.
Guillon, J. M., & Raquin, C. (2002). Environmental sex determination in the genus Equisetum: Sugars induce male sex expression in cultured gametophytes. International Journal of Plant Science, 163, 825–830.
Haag, C. R., Sakwinska, O., & Ebert, D. (2003). Test of synergistic interactions between infection and inbreeding in Daphnia magna. Evolution, 57, 777–783.
Hadany, L., & Feldman, M. W. (2005). Evolutionary traction, the cost of adaptation and the evolution of sex. Journal of Evolutionary Biology, 18, 309–314.
Hakoyama, H., Nishimura, T., Matsubara, N., & Iguchi, K. (2001). Difference in parasite load and nonspecific immune reaction between sexual and gynogenetic forms of Carassius auratus. Biological Journal of the Linnaean Society of London, 72, 401–407.
Haldane, J. B. S. (1922). Sex ratio and unisexual sterility in hybrid animals. Journal of Genetics, 12, 101–109.
Halkett, F., Simon, J.-C., & Balloux, F. (2005). Tackling the population genetics of clonal and partially clonal organisms. Trends in Ecology & Evolution, 20, 194–201.
Hamilton, W. D. (1980). Sex versus non-sex versus parasite. Oikos, 35, 282–290.
Hamilton, W. D., Axelrod, R., & Tanese, R. (1990). Sexual reproduction as an adaptation to resist parasites (a review). Proceedings of the National Academy of Sciences USA, 87, 3566–3573.
Hanley, K. A., Fisher, R. N., & Case, T. J. (1995). Lower mite infestations in an asexual gecko compared with its sexual ancestors. Evolution, 49, 418–426.
Heethoff, M., Domes, K., Laumann, M., Maraun, M., Norton, R. A., & Scheu, S. (2007). High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida). Journal of Evolutionary Biology, 20, 392–402.
Henry, L., Schwander, T., & Crespi, B. J. (2012). Deleterious mutation accumulation in asexual Timema stick insects. Molecular Biology and Evolution, 29, 401–408.
Hillis, D. M. (2007). Asexual evolution, can species exist without sex? Current Biology, 17, R543–R544.
Hörandl, E., Cosendai, A.-C., & Temsch, E. (2008). Understanding the geographic distributions of apomictic plants, a case for a pluralistic approach. Plant Ecology and Diversity, 2, 309–320.
Howard, R. S., & Lively, C. M. (1994). Parasitism, mutation accumulation and the maintenance of sex. Nature, 367, 554–557.
Johnson, S. J. (2000). Populations structure, parasitism and survivorship of sexual and asexual autodiploid parthenogenetic Campeloma limum. Evolution, 54, 167–175.
Judson, O. P., & Normark, B. B. (1996). Ancient asexual scandals. Trends in Ecology & Evolution, 11, A41–A46.
Kearney, M. (2005). Hybridization, glaciation and geographical parthenogenesis. Trends in Ecology & Evolution, 20, 495.
Kearney, M., & Shine, R. (2005). Lower fecundity in parthenogenetic geckos than sexual relatives in the Australian arid zone. Journal of Evolutionary Biology, 18, 609–618.
Keightley, P. D., & Eyre-Walker, A. (2000). Deleterious mutations and the evolution of sex. Science, 290, 331–333.
Kondrashov, A. S. (1993). Classification of hypotheses on the advantage of amphimixis. Journal of Heredity, 84, 372–387.
Kondrashov, A. S. (1994). The asexual ploidy cycle and the origin of sex. Nature, 370, 213–216.
Ladle, R. J. (1992). Parasites and sex, catching the red queen. Trends in Ecology & Evolution, 7, 405–408.
Lamatsch, D. K., Lampert, K. P., Fischer, P., Epplen, J. T., Nanda, I., Schmid, M., et al. (2007). Automictic reproduction in interspecific hybrids of poeciliid fish. Current Biology, 17, 1948–1953.
Lattorff, H. M. G., Moritz, R. F. A., & Fuchs, S. (2005). A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity, 94, 533–537.
Lawrence, J. G. (1999). Gene transfer, speciation, and the evolution of bacterial genomes. Current Opinion Microbiology, 2, 519–523.
Lesbarrères, D. (2011). Sex or no sex, reproduction is not the question. BioEssays, 33, 818.
Lively, C. M. (2009). The maintenance of sex, host–parasite coevolution with density-dependent virulence. Journal of Evolutionary Biology, 22, 2086–2093.
Lively, C. M., Craddock, C., & Vrijenhoek, R. C. (1990). Red queen hypothesis supported by parasitism in sexual and clonal fish. Nature, 344, 864–867.
Lively, C. M., & Jokela, J. (2002). Temporal and spatial distributions of parasites and sex in a freshwater snail. Evolutionary Ecological Research, 4, 219–226.
Lively, C. M., & Lloyd, D. G. (1990). The cost of biparental sex under individual selection. American Naturalist, 135, 489–500.
Lodé, T. (2011). Sex is not a solution for reproduction, the libertine bubble theory. BioEssays, 33, 419–422.
Lodé, T. (2012a). Sex and the origin of genetic exchanges. Trends in Evolutionary Biology, 2012(4), e1.
Lodé, T. (2012b). For quite a few chromosomes more: The origin of eukaryotes. Journal of Molecular Biology, 423, 135–142.
Lodé, T. (2012c). Have sex or not? Lessons from bacteria. Sexual Development, 6, 325–328.
Loxdale, H. D., & Lushai, G. (2003). Rapid changes in clonal lines, the death of a ‘sacred cow. Biological Journal of the Linnaean Society, 79, 3–16.
Lunt, D. H. (2008). Genetic tests of ancient asexuality in root knot nematodes reveal 536 recent hybrid origins. BMC Evolutionary Biology, 8, 194.
Lushai, G., Loxdale, H. D., & Allen, J. A. (2003). The dynamic clonal genome and its adaptive potential. Biological Journal of the Linnaean Society of London, 79, 193–208.
Lynch, M. (1984). Destabilizing hybridization, general-purpose genotypes, and geographic parthenogenesis. Quaternary Review of Biology, 59, 257–290.
Mable, K. (2007). Sex in the postgenomic era. Trends in Ecology & Evolution, 2, 559–561.
Mallet, J. (2007). Hybrid speciation. Nature, 446, 279–283.
Marin, I., & Baker, B. S. (1998). The evolutionary dynamics of sex determination. Science, 281, 1990–1994.
Mark-Welch, J. L., Mark-Welch, D. B., & Meselson, M. (2004). Cytogenetic evidence for asexual evolution of bdelloid rotifers. Proceedings of the National Academy of Sciences USA, 101, 1618–1621.
Mark-Welch, D., & Meselson, M. (2000). Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science, 288, 1211–1215.
Martens, K., Rossetti, G., & Home, D. J. (2003). How ancient are ancient asexuals? Proceedings of the National Academy of Sciences USA, 270, 723–729.
Martin, W. F. (2011). Early evolution without a tree of life. Biology Direct, 6, 36.
Matheos, M., & Vrijenhoek, R. C. (2007). Ancient versus reticulate origin of hemiclonal lineage. Evolution, 56, 985–992.
Maynard-Smith, J. (1978). The evolution of sex. Cambridge, UK: Cambridge University Press.
McDaniel, L. D., Young, E., Delaney, J., Ruhnau, F., Ritchie, K. B., & Paul, J. H. (2010). High frequency of horizontal gene transfer in the oceans. Science, 330, 50.
McDermott, S. R., & Noor, M. A. F. (2010). The role of meiotic drive in hybrid male sterility. Philosophical Transactions of the Royal Society B, 365, 1265–1272.
Morran, L. T., Schmidt, O. G., Gelarden, I. A., Parrish, R. C., I. I., & Lively, C. M. (2011). Running with the red queen, host-parasite coevolution selects for biparental sex. Science, 333, 216–218.
Muller, H. J. (1964). The relation of mutation to mutational advance. Mutation Research, 1, 2–9.
Normark, B. B., Judson, O. P., & Moran, N. A. (2003). Genomic signatures of ancient asexual lineages. Biological Journal of the Linnaean Society of London, 79, 69–84.
Nygren, A., & Sundberg, P. (2003). Phylogeny and evolution of reproductive modes in Autolytinae Syllidae, Annelida. Molecular Phylogeny and Evolution, 29, 235–249.
Ochman, H., Lerat, E., & Daubin, V. (2005). Examining bacterial species under the specter of gene transfer and exchange. Proceedings of the National Academy of Sciences USA, 102, 6595–6599.
Otto, S. P. (2009). The evolutionary enigma of sex. American Naturalist, 174, S1–S14.
Pagano, A., Dubois, A., Lesbarrères, D., & Lodé, T. (2003). Frog alien species, a way for genetic invasion? Comptes-Rendus Biologies, 326, 85–92.
Pagano, A., Lesbarrères, D., O’hara, R., Crivelli, A., Veith, M., Lodé, T., et al. (2008). Geographical and ecological distributions of frog hemiclones suggest occurrence of both “General Purpose Genotype” and “Frozen Niche Variation” clones. Journal of Zoological Systems in Evolutionary Research, 46, 162–168.
Pal, C., Macia, M., Oliver, A., Schacher, I., & Buckling, A. (2007). Coevolution with viruses drives the evolution of bacterial mutation rates. Nature, 450, 1079–1081.
Parker, E. D, Jr, & Selander, R. K. (1976). The organization of genetic diversity in the parthenogenetic lizard Cnemidophorus tesselatus. Genetics, 84, 791–805.
Parnell, J. J., Rompato, G., Latta IV, L. C., Pfrender, M. E., Van Nostrand, J. D., He, Z., Zhou, J., Andersen, G., Champine, P., Balasubramanian, G., & Weimer, B. C. (2010). Functional biogeography as evidence of gene transfer in hypersaline microbial communities. PLoS One, 5, e12919. doi:10.1371/journal.pone.0012919.
Passamonti, M., Mantovani, B., & Scali, V. (2004). Phylogeny and karyotype evolution of the Iberian Leptynia attenuata species complex (Insecta Phasmatodea). Molecular Phylogeny and Evolution, 30, 87–96.
Penny, D. (1985). The evolution of meiosis and sexual reproduction. Biological Journal of the Linnaean Society of London, 25, 209–220.
Phadnis, N., & Orr, H. A. (2009). A single gene causes both male sterility and segregation distortion in Drosophila hybrids. Science, 323, 376–379.
Presgraves, D. C. (2007). Speciation genetics, epistasis, conflict and the origin of species. Current Biology, 17, R125–R127.
Quarin, C. L., Espinoza, F., Martinez, E. J., Pessino, S. C., & Bovo, O. A. (2001). A rise of ploidy level induces the expression of apomixis in Paspalum notatum. Sex Plant Reproduction, 13, 243–249.
Ramesh, M. A., Malik, S., & Logsdon, J. M. (2005). A phylogenomic inventory of meiotic genes, evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology, 15, 185–191.
Redfield, R. (2001). Do bacteria have sex? Nature Reviews of Genetics, 2, 634–639.
Rice, W. R. (2000). Dangerous liaisons. Proceedings of the National Academy of Sciences USA, 97, 12953–12955.
Rice, W. R. (2002). Experimental tests of the adaptive significance of sexual recombination. Nature Reviews of Genetics, 3, 241–251.
Rieseberg, L., & Willis, J. H. (2007). Plant speciation. Science, 317, 910–914.
Robinson, M. T., Weeks, A. R., & Hoffmann, A. A. (2002). Geographic patterns of clonal diversity in the earth mite species Penthaleus major with particular emphasis on species margins. Evolution, 56, 1160–1167.
Salathé, P., & Ebert, D. (2003). The effects of parasitism and inbreeding on the competitive ability in Daphnia magna, evidence for synergistic epistasis. Journal of Evolutionary Biology, 16, 976–985.
Schaefer, I., Domes, K., Heethoff, M., Schneider, K., Schön, I., Norton, R. A., et al. (2006). No evidence for the “Meselson effect” in parthenogenetic oribatid mites (Oribatida, Acari). Journal of Evolutionary Biology, 19, 184–193.
Schartl, M., Wilde, B., Schlupp, I., & Parzefall, J. (1995). Evolutionary origin of a parthenoform, the Amazon Molly Poecilia formosa, on the basis of a molecular genealogy. Evolution, 49, 827–835.
Schley, D., Doncaster, C., & Slutkin, T. (2004). Population models of sperm-dependent parthenogenesis. Journal of Theoretical Biology, 229, 559–572.
Schmeller, D. S., O’Hara, R., & Kokko, H. (2005). Male adaptive stupidity, male mating pattern in hybridogenetic frogs. Evolutionary Ecological Research, 7, 1039–1050.
Schmidt, B. R. (1993). Are hybridogenetic frogs cyclical parthenogens? Trends in Ecology & Evolution, 8, 271–273.
Schön, I., Butlin, R. K., Griffiths, H. I., & Martens, K. (1998). Slow evolution in an ancient asexual ostracod. Proceedings of the Royal Society of London B, 265, 235–242.
Schön, I., & Martens, K. (2003). No slave to sex. Proceedings of the Royal Society of London B, 270, 827–833.
Schultz, R. J. (1971). Special adaptive problems associated with unisexual fishes. American Zoologist, 11, 351–360.
Schurko, A. M., & Logsdon, J. M, Jr. (2008). Using a meiosis detection toolkit to investigate ancient asexual “scandals”. BioEssays, 30, 579–589.
Schwander, T., & Crespi, B. J. (2008). Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution, 63, 84–103.
Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198–207.
Simon, J. C., Delmotte, F., Rispe, C., & Crease, T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives, the possible routes to parthenogenesis in animals. Biological Journal of the Linnaean Society of London, 79, 151–163.
Slobodchikoff, C. N., & Daly, H. V. (1971). Systematic and evolutionary implications of parthenogenesis in the Hymenoptera. American Zoologist, 11, 273–282.
Smith, R. J., Kamiya, T., & Horne, D. J. (2006). Living males of the ‘ancient asexual’ Darwinulidae (Ostracoda, Crustacea). Proceedings of the National Academy of Sciences USA, 273, 1569–1578.
Sun, S., & Heitman, J. (2011). Is sex necessary? BMC Biology, 9, 56.
Suomalainen, E. (1962). Significance of Parthenogenesis in the Evolution of Insects. Annual Review of Entomology, 7, 349–366.
Suomalainen, E., Saura, E., & Lokki, J. (1976). Evolution of parthenogenetic insects. Evolutionary Biology, 9, 209–257.
Tobler, M., & Schlupp, I. (2005). Parasites in sexual and asexual mollies Poecilia, Poeciliidae, Teleostei, a case for the Red Queen? Biology Letters, 1, 166–168.
Uyenoyama, M. K. (1984). On the evolution of parthenogenesis, A genetic representation of the “cost of meiosis”. Evolution, 38, 87–102.
Venditti, P. C., Meade, A., & Pagel, M. (2010). Phylogenies reveal new interpretation of speciation and the Red Queen. Nature, 463, 349–352.
Vorburger, C. (2001). Heterozygous fitness effects of clonally transmitted genomes in waterfrogs. Journal of Evolutionary Biology, 14, 602–610.
Vorburger, C., Sunnucks, P., & Ward, S. A. (2003). Explaining the coexistence of asexuals with their sexual progenitors, no evidence for general-purpose genotypes in obligate parthenogens of the peach-potato aphid, Myzus persicae. Ecology Letters, 6, 1091–1098.
Vos, M. (2009). Why do bacteria engage in homologous recombination? Trends in Microbiology, 17, 226–232.
Vrijenhoek, R. C. (1994). Unisexual fish, model systems for studying ecology and evolution. Annual Review of Ecological System, 25, 71–96.
Vrijenhoek, R. C. (1998). Animal clones and diversity. Are natural clones generalists or specialists? BioScience, 48, 617–628.
Watson, R. A., Weinreich, D. M., & Wakeley, J. (2011). Genomes structure and the benefit of sex. Evolution, 65, 523–536.
Wenseleers, T., & Van Oystaeyen, A. (2011). Unusual modes of reproduction in social insects: Shedding light on the evolutionary paradox of sex. BioEssays, 33, 927–937.
Wilkinson, G. S., & Fry, C. L. (2001). Meiotic drive alters sperm competitive ability in stalk-eyed flies. Proceedings of the Royal Society of London B, 268, 2559–2564.
Williams, G. C. (1975). Sex and evolution. Princeton: Princeton University Press.
Woolley, S. C., Sakata, J. T., & Crews, D. (2004). Tracing the Evolution of Brain and Behavior Using Two Related Species of Whiptail Lizards: Cnemidophorus uniparens and Cnemidophorus inornatus. Institute for Laboratory Animal Research Journal, 45, 46–53.
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I would like to thank David Crews and two anonymous referees for helpful suggestions.
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Lodé, T. Adaptive Significance and Long-Term Survival of Asexual Lineages. Evol Biol 40, 450–460 (2013). https://doi.org/10.1007/s11692-012-9219-y
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DOI: https://doi.org/10.1007/s11692-012-9219-y