Despite its inherent costs, sexual reproduction is ubiquitous in nature, and the mechanisms to protect it from a competitive displacement by asexuality remain unclear. Popular mutation-based explanations, like the Muller's ratchet and the Kondrashov's hatchet, assume that purifying selection may not halt the accumulation of deleterious mutations in the nonrecombining genomes, ultimately leading to their degeneration. However, empirical evidence is scarce and it remains particularly unclear whether mutational degradation proceeds fast enough to ensure the decay of clonal organisms and to prevent them from outcompeting their sexual counterparts. To test this hypothesis, we jointly analysed the exome sequences and the fitness-related phenotypic traits of the sexually reproducing fish species and their clonal hybrids, whose evolutionary ages ranged from F1 generations to 300 ky. As expected, mutations tended to accumulate in the clonal genomes in a time-dependent manner. However, contrary to the predictions, we found no trend towards increased nonsynonymity of mutations acquired by clones, nor higher radicality of their amino acid substitutions. Moreover, there was no evidence for fitness degeneration in the old clones compared with that in the younger ones. In summary, although an efficacy of purifying selection may still be reduced in the asexual genomes, our data indicate that its efficiency is not drastically decreased. Even the oldest investigated clone was found to be too young to suffer fitness consequences from a mutation accumulation. This suggests that mechanisms other than mutation accumulation may be needed to explain the competitive advantage of sex in the short term.

Department of Biology and Ecology University of Ostrava Ostrava Czechia

Department of Ecology University of Prešov Prešov Slovakia

Institute of Animal Physiology and Genetics Czech Academy of Science Liběchov Czechia

Institute of Molecular Genetics Czech Academy of Science Prague Czechia

Institute of Vertebrate Biology Czech Academy of Science Brno Czechia

Museum of Natural History University of Wrocław Wrocław Poland

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Allen, J. M. , Light, J. E. , Perotti, M. A. , Braig, H. R. , & Reed, D. L. (2009). Mutational meltdown in primary endosymbionts: Selection limits Muller’s Ratchet. PLoS One, 4(3), e4969 10.1371/journal.pone.0004969 PubMed DOI PMC

Ament‐Velásquez, S. L. , Figuet, E. , Ballenghien, M. , Zattara, E. E. , Norenburg, J. L. , Fernández‐Álvarez, F. A. , … Galtier, N. (2016). Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): Hybridization, polyploidy and the Meselson effect. Molecular Ecology, 25(14), 3356–3369. 10.1111/mec.13717 PubMed DOI

Andersson, D. I. , & Hughes, D. (1996). Muller’s ratchet decreases fitness of a DNA‐based microbe. Proceedings of the National Academy of Sciences, 93(2), 906–907. 10.1073/pnas.93.2.906 PubMed DOI PMC

Auwera, G. A. , Carneiro, M. O. , Hartl, C. , Poplin, R. , del Angel, G. , Levy‐Moonshine, A. , … DePristo, M. A. (2013). From FastQ data to high confidence variant calls: The Genome Analysis Toolkit best practices pipeline. Current Protocols in Bioinformatics, 43, 1–33. 10.1002/0471250953.bi1110s43 PubMed DOI PMC

Bartoš, O. , Röslein, J. , Kotusz, J. , Paces, J. , Pekárik, L. , Petrtýl, M. , … Janko, K. (2019). The legacy of sexual ancestors in phenotypic variability, gene expression and homoeolog regulation of asexual hybrids and polyploids. Molecular Biology and Evolution, 36(9), 1902–1920. 10.1093/molbev/msz114 PubMed DOI PMC

Bates, D. , Maechler, M. , Bolker, B. , & Walker, S. (2015). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67(1), 1–48. 10.18637/jss.v067.i01 DOI

Beukeboom, L. W. , & Vrijenhoek, R. C. (1998). Evolutionary genetics and ecology of sperm dependent parthenogenesis. Journal of Evolutionary Biology, 11, 755–782. 10.1007/s000360050117 DOI

Birky, C. W. (2010). Positively negative evidence for asexuality. Journal of Heredity, 101(Supplement 1), S42–S45. 10.1093/jhered/esq014 PubMed DOI

Birky, C. W. , & Barraclough, T. G. (2009). Asexual Speciation In Schön I., Martens K., & van Dijk P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis (pp. 201–216). Dordrecht, Heidelberg, London, New York: Springer.

Bobyrev, A. , Burmensky, V. , Vasilev, V. , Kriksunov, E. , & Lebedeva, E. (2003). Coexistence of triploid and diploid forms of spined loach, Cobitis taenia: A model‐based approach. Folia Biologica, 51(Suppl.), 55–60. PubMed

Bohlen, J. (1999). Reproduction of spined loach, Cobitis taenia,(Cypriniformes; Cobitidae) under laboratory conditions. Journal of Applied Ichthyology., 15(2), 49–53.10.1046/j.1439-0426.1999.00122.x DOI

Brandt, A. , Schaefer, I. , Glanz, J. , Schwander, T. , Maraun, M. , Scheu, S. , & Bast, J. (2017). Effective purifying selection in ancient asexual oribatid mites. Nature Communications, 8(1), 873 10.1038/s41467-017-01002-8 PubMed DOI PMC

Burgarella, C. , Gayral, P. , Ballenghien, M. , Bernard, A. , David, P. , Jarne, P. , … Glémin, S. (2015). Molecular evolution of freshwater snails with contrasting mating systems. Molecular Biology and Evolution, 32(9), 2403–2416. 10.1093/molbev/msv121 PubMed DOI

Chao, L. (1990). Fitness of RNA virus decreased by Muller’s ratchet. Nature, 348(6300), 454–455. 10.1038/348454a0 PubMed DOI

Choleva, L. , Janko, K. , De Gelas, K. , Bohlen, J. , Šlechtová, V. , Rábová, M. , & Ráb, P. (2012). Synthesis of clonality and polyploidy in vertebrate animals by hybridization between two sexual species. Evolution, 66(7), 2191–2203. 10.1111/j.1558-5646.2012.01589.x PubMed DOI

Choleva, L. , Musilova, Z. , Kohoutova‐Sediva, A. , Paces, J. , Rab, P. , & Janko, K. (2014). Distinguishing between incomplete lineage sorting and genomic introgressions: Complete fixation of allospecific mitochondrial DNA in a sexually reproducing fish (Cobitis; Teleostei), despite clonal reproduction of hybrids. PLoS One, 9(6), e80641 10.1371/journal.pone.0080641 PubMed DOI PMC

Conesa, A. , Gotz, S. , Garcia‐Gomez, J. M. , Terol, J. , Talon, M. , & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21(18), 3674–3676. 10.1093/bioinformatics/bti610 PubMed DOI

Dedukh, D. , Majtánová, Z. , Marta, A. , Pšenička, M. , Kotusz, J. , Klíma, Jiří. , Juchno, D. , Boron, A. , Janko, K . (2020). Parthenogenesis as a Solution to Hybrid Sterility: the Mechanistic Basis of Meiotic Distortions in Clonal and Sterile Hybrids. Genetics, genetics.302988.2019 10.1534/genetics.119.302988.(Early online June 9, 2020). PubMed DOI PMC

DePristo, M. A. , Banks, E. , Poplin, R. , Garimella, K. V. , Maguire, J. R. , Hartl, C. , … Daly, M. J. (2011). A framework for variation discovery and genotyping using next‐generation DNA sequencing data. Nature Genetics, 43(5), 491–498. 10.1038/ng.806 PubMed DOI PMC

Doncaster, C. P. , Pound, G. E. , & Cox, S. J. (2000). The ecological cost of sex. Nature, 404(6775), 281–285. 10.1038/35005078 PubMed DOI

Eyre‐Walker, A. , & Keightley, P. D. (2009). Estimating the rate of adaptive molecular evolution in the presence of slightly deleterious mutations and population size change. Molecular Biology and Evolution, 26(9), 2097–2108. 10.1093/molbev/msp119 PubMed DOI

Fedorčák, J. , Koščo, J. , Halačka, K. , & Manko, P. (2017). Growth differences in different biotypes of the hybrid complex of Cobitis elongatoides × Cobitis tanaitica (Actinopterygii: Cypriniformes: Cobitidae) in the Okna River (Danube River basin), Slovakia. Acta Ichthyologica Et Piscatoria, 47, 125–132. 10.3750/AIEP/02059 DOI

Flot, J.‐F. , Hespeels, B. , Li, X. , Noel, B. , Arkhipova, I. , Danchin, E. G. J. , … Van Doninck, K. (2013). Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga . Nature, 500(7463), 453–457. 10.1038/nature12326 PubMed DOI

Fontaneto, D. , Tang, C. Q. , Obertegger, U. , Leasi, F. , & Barraclough, T. G. (2012). Different diversification rates between sexual and asexual organisms. Evolutionary Biology, 39(2), 262–270. 10.1007/s11692-012-9161-z DOI

Gayral, P. , Melo‐Ferreira, J. , Glémin, S. , Bierne, N. , Carneiro, M. , Nabholz, B. , … Galtier, N. (2013). Reference‐free population genomics from next‐generation transcriptome data and the vertebrate‐invertebrate gap. PLoS Genetics, 9(4), e1003457 https://journals.plos.org/plosgenetics/article/citation?id=10.1371/journal.pgen.1003457 PubMed PMC

Goddard, M. R. , Godfray, H. C. J. , & Burt, A. (2005). Sex increases the efficacy of natural selection in experimental yeast populations. Nature, 434(7033), 636–640. 10.1038/nature03405 PubMed DOI

Guex, G.‐D. , Hotz, H. , & Semlitsch, R. D. (2002). Deleterious alleles and differential viability in progeny of natural hemiclonal frogs. Evolution, 56(5), 1036–1044. 10.1111/j.0014-3820.2002.tb01414.x PubMed DOI

Guindon, S. , Dufayard, J.‐F. , Lefort, V. , Anisimova, M. , Hordijk, W. , & Gascuel, O. (2010). New algorithms and methods to estimate maximum‐likelihood phylogenies: assessing the performance of phyml 3.0. Systematic Biology, 59(3), 307–321. 10.1093/sysbio/syq010 PubMed DOI

Halačka, K. , Lusková, V. , & Lusk, S. (2000). Fecundity of Cobitis elongatoides in the Nová Říše reservoir. Folia Zoologica, 49, 141–150.

Halligan, D. L. , & Keightley, P. D. (2003). How many lethal alleles? Trends in Genetics, 19(2), 57–59. 10.1016/S0168-9525(02)00045-8 PubMed DOI

Hamilton, W. D. (1980). Sex versus non‐sex versus parasite. Oikos, 35(2), 282–290. 10.2307/3544435 DOI

Hartfield, M. , & Keightley, P. D. (2012). Current hypotheses for the evolution of sex and recombination. Integrative Zoology, 7(2), 192–209. 10.1111/j.1749-4877.2012.00284.x PubMed DOI

Henry, L. , Schwander, T. , & Crespi, B. J. (2012). Deleterious mutation accumulation in asexual Timema stick insects. Molecular Biology and Evolution, 29(1), 401–408. 10.1093/molbev/msr237 PubMed DOI

Hellriegel, B. , & Reyer, H. U. (2000). Factors influencing the composition of mixed populations of a hemiclonal hybrid and its sexual host. Journal of Evolutionary Biology., 13(6), 906–918.10.1046/j.1420-9101.2000.00235.x DOI

Hollister, J. D. , Greiner, S. , Wang, W. , Wang, J. , Zhang, Y. , Wong, G.‐S. , … Johnson, M. T. J. (2015). Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera . Molecular Biology and Evolution, 32(4), 896–905. 10.1093/molbev/msu345 PubMed DOI

Howe, D. , & Denver, D. (2008). Muller’s Ratchet and compensatory mutation in Caenorhabditis briggsae mitochondrial genome evolution. BMC Evolutionary Biology, 8(1), 62 10.1186/1471-2148-8-62 PubMed DOI PMC

Janko, K. (2014). Let us not be unfair to asexuals: Their ephemerality may be explained by neutral models without invoking any evolutionary constraints of asexuality. Evolution, 68(2), 569–576. 10.1111/evo.12293 PubMed DOI

Janko, K. , Bohlen, J. , Lamatsch, D. , Flajšhans, M. , Epplen, J. T. , Ráb, P. , … Šlechtová, V. (2007). The gynogenetic reproduction of diploid and triploid hybrid spined loaches (Cobitis: Teleostei), and their ability to establish successful clonal lineages—on the evolution of polyploidy in asexual vertebrates. Genetica, 131(2), 185–194. 10.1007/s10709-006-9130-5 PubMed DOI

Janko, K. , Culling, M. A. , Rab, P. , & Kotlik, P. (2005). Ice age cloning‐comparison of the Quaternary evolutionary histories of sexual and clonal forms of spiny loaches (Cobitis; Teleostei) using the analysis of mitochondrial DNA variation. Molecular Ecology, 14(10), 2991–3004. 10.1111/j.1365-294X.2005.02583.x PubMed DOI

Janko, K. , Drozd, P. , & Eisner, J. (2011). Do clones degenerate over time? Explaining the genetic variability of asexuals through population genetic models. Biology Direct, 6, 17 10.1186/1745-6150-6-17 PubMed DOI PMC

Janko, K. , Drozd, P. , Flegr, J. , & Pannell, J. R. (2008). Clonal turnover versus clonal decay: A null model for observed patterns of asexual longevity, diversity and distribution. Evolution, 62(5), 1264–1270. 10.1111/j.1558-5646.2008.00359.x PubMed DOI

Janko, K. , Flajšhans, M. , Choleva, L. , Bohlen, J. , Šlechtová, V. , Rábová, M. , … Ráb, P. (2007). Diversity of European spined loaches (genus Cobitis L.): An update of the geographic distribution of the Cobitis taenia hybrid complex with a description of new molecular tools for species and hybrid determination. Journal of Fish Biology, 71, 387–408. 10.1111/j.1095-8649.2007.01663.x DOI

Janko, K. , Kotusz, J. , De Gelas, K. , Šlechtová, V. , Opoldusová, Z. , Drozd, P. , … Baláž, M. (2012). Dynamic formation of asexual diploid and polyploid lineages: Multilocus analysis of Cobitis reveals the mechanisms maintaining the diversity of clones. PLoS One, 7(9), e45384 10.1371/journal.pone.0045384 PubMed DOI PMC

Janko, K. , Pačes, J. , Wilkinson‐Herbots, H. , Costa, R. J. , Roslein, J. , Drozd, P. , … Choleva, L. (2018). Hybrid asexuality as a primary postzygotic barrier between nascent species: On the interconnection between asexuality, hybridization and speciation. Molecular Ecology, 27, 249–263. 10.1111/mec.14377 PubMed DOI PMC

Janko, K. , Vasil’ev, V. P. , Rab, P. , Rabova, M. , Slechtova, V. , & Vasil’eva, E. D. (2005). Genetic and morphological analyses of 50‐chromosome spined loaches (Cobitis, Cobitidae, Pisces) from the Black Sea basin that are morphologically similar to C. taenia, with the description of a new species. Folia Zoologica, 54(4), 405–420.

Johnson, M. T. J. , FitzJohn, R. G. , Smith, S. D. , Rausher, M. D. , & Otto, S. P. (2011). Loss of sexual recombination and segregation is associated with increased diversification in evening primroses. Evolution, 65(11), 3230–3240. 10.1111/j.1558-5646.2011.01378.x PubMed DOI PMC

Johnson, S. G. , & Howard, R. S. (2007). Contrasting patterns of synonymous and nonsynonymous sequence evolution in asexual and sexual freshwater snail lineages. Evolution, 61(11), 2728–2735. 10.1111/j.1558-5646.2007.00233.x PubMed DOI

Juchno, D. , Arai, K. , Boroń, A. , & Kujawa, R. (2016). Meiotic chromosome configurations in oocytes of Cobitis taenia and its polyploid hybrids. Ichthyological Research, 64(2), 240–243. 10.1007/s10228-016-0556-1 DOI

Juchno, D. , & Boron, A. (2010). Fecundity of the spined loach, Cobitis taenia (Pisces, Cobitidae) and natural allopolyploids of Cobitis from a diploid‐polyploid population. Folia Zoologica. Retrieved from http://www.highbeam.com/doc/1P3‐2013942551.html

Juchno, D. , Jabłońska, O. , Boroń, A. , Kujawa, R. , Leska, A. , Grabowska, A. , … Lao, M. (2014). Ploidy‐dependent survival of progeny arising from crosses between natural allotriploid Cobitis females and diploid C. taenia males (Pisces, Cobitidae). Genetica, 142(4), 351–359. 10.1007/s10709-014-9779-0 PubMed DOI

Kondrashov, A.S. (1993). Classification of hypotheses on the advantage of amphimixis. Journal of Heredity, 84(5), 372–387. 10.1093/oxfordjournals.jhered.a111358 PubMed DOI

Kondrashov, A. S. (1982). Selection against harmful mutations in large sexual and asexual populations. Genetics Research., 40(3), 325–332. PubMed

Kotusz, J. (2008). Morphological relationships between polyploid hybrid spined loaches of the genus Cobitis (Teleostei: Cobitidae) and their parental species. Annales Zoologici, 58, 891–905. 10.3161/000345408X396800 DOI

Kotusz, J. , Popiołek, M. , Drozd, P. , De Gelas, K. , Šlechtová, V. , & Janko, K. (2014). Role of parasite load and differential habitat preferences in maintaining the coexistence of sexual and asexual competitors in fish of the Cobitis taenia hybrid complex. Biological Journal of the Linnean Society, 113(1), 220–235. 10.1111/bij.12329 DOI

Lefort, V. , Longueville, J.‐E. , & Gascuel, O. (2017). SMS: Smart model selection in phyml . Molecular Biology and Evolution, 34(9), 2422–2424. 10.1093/molbev/msx149 PubMed DOI PMC

Leslie, J. F., & Vrijenhoek, R. C. (1978). Genetic dissection of clonally inherited genomes of poeciliopsis. I. Linkage analysis and preliminary assessment of deleterious gene loads. Genetics. 90(4), 801–811. PubMed PMC

Leslie, J. F. , & Vrijenhoek, R. C. (1980). Consideration of Muller's ratchet mechanism through studies of genetic linkage and genomic compatibilities in clonally reproducing Poeciliopsis. Evolution., 34(6), 1105–1115.10.1111/j.1558-5646.1980.tb04051.x PubMed DOI

Li, H. , & Durbin, R. (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics, 25(14), 1754–1760. 10.1093/bioinformatics/btp324 PubMed DOI PMC

Liu, H.‐M. , Dyer, R. J. , Guo, Z.‐Y. , Meng, Z. , Li, J.‐H. , & Schneider, H. (2012). The evolutionary dynamics of apomixis in ferns: A case study from polystichoid ferns. Journal of Botany, 2012, 1–11. 10.1155/2012/510478 DOI

Loewe, L. , & Lamatsch, D. K. (2008). Quantifying the threat of extinction from Muller’s ratchet in the diploid Amazon molly (Poecilia formosa). BMC Evolutionary Biology, 8(1), 88 10.1186/1471-2148-8-88 PubMed DOI PMC

Lundmark, M. (2006). Polyploidization, hybridization and geographical parthenogenesis. Trends in Ecology & Evolution, 21(1), 9 10.1016/j.tree.2005.10.007 PubMed DOI

Maciak, S. , Janko, K. , Kotusz, J. , Choleva, L. , Boroń, A. , Juchno, D. , … Konarzewski, M. (2011). Standard Metabolic Rate (SMR) is inversely related to erythrocyte and genome size in allopolyploid fish of the Cobitis taenia hybrid complex. Functional Ecology, 25(5), 1072–1078. 10.1111/j.1365-2435.2011.01870.x DOI

Maciver, S. K. (2016). Asexual amoebae escape Muller’s ratchet through polyploidy. Trends in Parasitology, 32(11), 855–862. 10.1016/j.pt.2016.08.006 PubMed DOI

Majtánová, Z. , Choleva, L. , Symonová, R. , Ráb, P. , Kotusz, J. , Pekárik, L. , & Janko, K. (2016). Asexual reproduction does not apparently increase the rate of chromosomal evolution: Karyotype stability in diploid and triploid clonal hybrid fish (Cobitis, Cypriniformes, Teleostei). PLoS One, 11(1), e0146872 10.1371/journal.pone.0146872 PubMed DOI PMC

McDonald, M. J. , Rice, D. P. , & Desai, M. M. (2016). Sex speeds adaptation by altering the dynamics of molecular evolution. Nature, 531(7593), 233–236. PubMed PMC

McKenna, A. , Hanna, M. , Banks, E. , Sivachenko, A. , Cibulskis, K. , Kernytsky, A. , … DePristo, M. A. (2010). The genome analysis toolkit: A MapReduce framework for analyzing next‐generation DNA sequencing data. Genome Research, 20(9), 1297–1303. 10.1101/gr.107524.110 PubMed DOI PMC

Naito, M. , & Pawlowska, T. E. (2016). Defying Muller’s Ratchet: Ancient heritable endobacteria escape extinction through retention of recombination and genome plasticity. MBio, 7(3), 10.1128/mBio.02057-15 PubMed DOI PMC

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(4), 954–963. 10.1093/molbev/msp300 PubMed DOI PMC

Otto, S. P. (2007). The evolutionary consequences of polyploidy. Cell, 131(3), 452–462. 10.1016/j.cell.2007.10.022 PubMed DOI

Otto, S. P. , & Whitton, J. (2000). Polyploid incidence and evolution. Annual Review of Genetics, 34, 401–437, 10.1146/annurev.genet.34.1.401 PubMed DOI

Paland, S. , Colbourne, J. K. , & Lynch, M. (2005). Evolutionary history of contagious asexuality in Daphnia pulex . Evolution, 59(4), 800–813. 10.1111/j.0014-3820.2005.tb01754.x PubMed DOI

Paland, S. , & Lynch, M. (2006). Transitions to asexuality result in excess amino acid substitutions. Science, 311(5763), 990–992. 10.1126/science.1118152 PubMed DOI

Peck, J. R. , Yearsley, J. M. , & Waxman, D. (1998). Explaining the geographic distributions of sexual and asexual populations. Nature, 391(6670), 889–892. 10.1038/36099 DOI

Pellino, M. , Hojsgaard, D. , Schmutzer, T. , Scholz, U. , Hörandl, E. , Vogel, H. , & Sharbel, T. F. (2013). Asexual genome evolution in the apomictic Ranunculus auricomus complex: Examining the effects of hybridization and mutation accumulation. Molecular Ecology, 22(23), 5908–5921. 10.1111/mec.12533 PubMed DOI

Pertea, G. (2015). fqtrim: v0.9.4 release. Zenodo. doi: 10.5281/zenodo.20552 DOI

Pinheiro, J. , Bates, D. , DebRoy, S. , Sarkar, D. , & R Core Team . (2016). Nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1. http://CRAN.R‐project.org/package=nlme

Pond, S. L. K. , Frost, S. D. W. , & Muse, S. V. (2005). hyphy: Hypothesis testing using phylogenies. Bioinformatics, 21(5), 676–679. 10.1093/bioinformatics/bti079 PubMed DOI

Pound, G. E. , Cox, S. J. , & Doncaster, C. P. (2004). The accumulation of deleterious mutations within the frozen niche variation hypothesis. Journal of Evolutionary Biology, 17(3), 651–662. 10.1111/j.1420-9101.2003.00690.x PubMed DOI

Quattro, J. M. , Avise, J. C. , & Vrijenhoek, R. C. (1992). An ancient clonal lineage in the fish genus Poeciliopsis (Atheriniformes: Poeciliidae). Proceedings of the National Academy of Sciences, 89(1), 348–352. 10.1073/pnas.89.1.348 PubMed DOI PMC

Ricker, W. E. (2010). Computation and interpretation of biological statistics of fish populations. Caldwell, NJ: The Blackburn Press.

Roach, K. C. , & Heitman, J. (2014). Unisexual reproduction reverses Muller’s ratchet. Genetics, 198(3), 1059–1069. 10.1534/genetics.114.170472 PubMed DOI PMC

Schön, I. , & Martens, K. (2003). No slave to sex. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1517), 827–833. 10.1098/rspb.2002.2314 PubMed DOI PMC

Schwander, T. , & Crespi, B. J. (2009). Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Molecular Ecology, 18(1), 28–42. 10.1111/j.1365-294X.2008.03992.x PubMed DOI

Sémon, M. , & Wolfe, K. H. (2007). Consequences of genome duplication. Current Opinion in Genetics & Development, 17(6), 505–512. 10.1016/j.gde.2007.09.007 PubMed DOI

Sharbrough, J. , Luse, M. , Boore, J. L. , Logsdon, J. M. Jr , & Neiman, M. (2018). Radical amino acid mutations persist longer in the absence of sex. Evolution, 72(4), 808–824. 10.1111/evo.13465 PubMed DOI

Shcherbakov, V. P. (2010). Biological species is the only possible form of existence for higher organisms: The evolutionary meaning of sexual reproduction. Biology Direct, 5, 14 10.1186/1745-6150-5-14 PubMed DOI PMC

Šimková, A. , Vojtek, L. , Halačka, K. , Hyršl, P. , & Vetešník, L. (2015). The effect of hybridization on fish physiology, immunity and blood biochemistry: A case study in hybridizing Cyprinus carpio and Carassius gibelio (Cyprinidae). Aquaculture., 435, 381–389.

Stajich, J. E. , Block, D. , Boulez, K. , Brenner, S. E. , Chervitz, S. A. , Dagdigian, C. , … Birney, E. (2002). The Bioperl toolkit: Perl modules for the life sciences. Genome Research, 12(10), 1611–1618. 10.1101/gr.361602 PubMed DOI PMC

Sunnucks, P. , England, P. R. , Taylor, A. C. , & Hales, D. F. (1996). Microsatellite and chromosome evolution of parthenogenetic sitobion aphids in Australia. Genetics, 144(2), 747–756. PubMed PMC

Suren, H. , Hodgins, K. A. , Yeaman, S. , Nurkowski, K. A. , Smets, P. , Rieseberg, L. H. , … Holliday, J. A. (2016). Exome capture from the spruce and pine giga‐genomes. Molecular Ecology Resources, 16, 1136–1146. 10.1111/1755-0998.12570 PubMed DOI

Tucker, A. E. , Ackerman, M. S. , Eads, B. D. , Xu, S. , & Lynch, M. (2013). Population‐genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex . Proceedings of the National Academy of Sciences, 110(39), 15740–15745. 10.1073/pnas.1313388110 PubMed DOI PMC

Vrijenhoek, R. C. , & Parker, E. D. (2009). Geographical parthenogenesis: general purpose genotypes and frozen niche variationIn Lost sex (pp. 99–131). Dordrecht: Springer.

Warren, W. C. , García‐Pérez, R. , Xu, S. , Lampert, K. P. , Chalopin, D. , Stöck, M. , … Schartl, M. (2018). Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nature Ecology and Evolution, 2(4), 669–679. 10.1038/s41559-018-0473-y PubMed DOI PMC

Weismann, A. (1889). The significance of sexual reproduction in the theory of natural selection In Poulton E., Schönland S., & Shipley A. (Eds.), Essays upon heredity and kindred biological problems, Vol. 1 (pp. 255–332). Oxford, UK: Clarendon Press.

West, S. , Lively, C. , & Read, A. (1999). A pluralist approach to sex and recombination. Journal of Evolutionary Biology, 12(6), 1003–1012. 10.1046/j.1420-9101.1999.00119.x DOI

Wertheim, J. O. , Murrell, B. , Smith, M. D. , Kosakovsky Pond, S. L. , & Scheffler, K. (2015). RELAX: Detecting Relaxed Selection in a Phylogenetic Framework. Molecular Biology and Evolution., 32(3), 820–832.10.1093/molbev/msu400 PubMed DOI PMC

Wetherington, J. D. , Kotora, K. E. , & Vrijenhoek, R. C. (1987). A test of the spontaneous heterosis hypothesis for unisexual vertebrates. Evolution, 41, 721–731. 10.1111/j.1558-5646.1987.tb05848.x PubMed DOI

Wetherington, J. D. , Weeks, S. C. , Kotora, K. E. , & Vrijenhoek, R. C. (1989). Genotypic and environmental components of variation in growth and reproduction of fish hemiclones (Poeciliopsis: Poeciliidae). Evolution, 43, 635–645. PubMed

Sperm-dependent asexual species and their role in ecology and evolution

Genome Fractionation and Loss of Heterozygosity in Hybrids and Polyploids: Mechanisms, Consequences for Selection, and Link to Gene Function

Challenges and Costs of Asexuality: Variation in Premeiotic Genome Duplication in Gynogenetic Hybrids from Cobitis taenia Complex