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Genome Evolution of Asexual Organisms and the Paradox of Sex in Eukaryotes

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Evolutionary Biology—A Transdisciplinary Approach

Abstract

The predominance of sex in eukaryotes is still enigmatic. Sex, a composed process of meiosis and mixis cycles, confers high costs but the selective advantages remain unclear. In this review, we focus on potentially detrimental effects of asexuality on genome evolution. Theory predicts that asexual lineages should suffer from lack of meiotic DNA repair, accumulation of deleterious mutations, proliferation of transposable elements, among others. Here, we compare the different genomic features, life cycles, developmental pathways, and cytological mechanisms in the major eukaryotic groups, i.e., in protists, animals, fungi, and plants. In general, it is difficult to disentangle lineage-specific features from general features of asexuality. In all groups, forms of asexuality are predominantly facultative or cyclical. A variety of mixed or partial sexual developmental pathways exists, maintaining some components of sexuality, while obligate asexuality appears to be rare in eukaryotes. The strongest theoretical prediction for negative consequences of asexuality is decreased effectiveness of selection compared to sexuality. While some studies have shown increased rates of mutation accumulation in asexuals, others using whole-genome comparisons did not find this pattern. Various mechanisms exist that can alleviate the negative consequences of accumulation of negative mutations. More empirical data are needed to understand comprehensively the role of genome evolution for the maintenance of sex.

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References

  • Adl SM, Bass D, Lane CE, Lukes J, Schoch CL, Smirnov A et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryotic Microbiol 66(1):4–119. https://doi.org/10.1111/jeu.12691

    Article  Google Scholar 

  • Aliyu OM, Schranz ME, Sharbel TF (2010) Quantitative variation for apomictic reproduction in the genus Boechera (Brassicaceae). Am J Bot 97(10):1719–1731. https://doi.org/10.3732/ajb.1000188

    Article  Google Scholar 

  • Ament-Velásquez SL, Figuet E, Ballenghien M, Zattara EE, Norenburg JL, Fernández-Álvarez FA et al (2016) Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus, Nemertea): hybridization, polyploidy and the Meselson effect. Mol Ecol 25:3356–3369

    Article  CAS  Google Scholar 

  • Arkhipova I, Meselson M (2000) Transposable elements in sexual and ancient asexual taxa. Proc Natl Acad Sci USA 97(26):14473–14477. https://doi.org/10.1073/pnas.97.26.14473

    Article  CAS  Google Scholar 

  • Arkhipova I, Meselson M (2005) Deleterious transposable elements and the extinction of asexuals. BioEssays 27:76–85

    Article  CAS  Google Scholar 

  • Arkhipova IR, Rodriguez F (2013) Genetic and epigenetic changes involving (retro)transposons in animal hybrids and polyploids. Cytogenet Genome Res 140:295–311

    Article  CAS  Google Scholar 

  • Asker S, Jerling L (1992) Apomixis in plants. CRC Press, Boca Raton

    Google Scholar 

  • Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM et al (2006) Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444:171–178

    Article  CAS  Google Scholar 

  • Azam F, Fenchel T, Field JG, Gray JS, Meyerreil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263

    Article  Google Scholar 

  • Bachtrog D, Hom E, Wong KM, Maside X, de Jong P (2008) Genomic degradation of a young Y chromosome in Drosophila miranda. Genome Biol. 9:R30

    Article  CAS  Google Scholar 

  • Bast J, Schaefer I, Schwander T, Maraun M, Scheu S, Kraaijeveld K (2016) No accumulation of transposable elements in asexual arthropods. Mol Biol Evol 33:697–706

    Article  CAS  Google Scholar 

  • Bast J, Parker DJ, Dumas Z, Jalvingh KM, Van Tran P, Jaron KS et al (2018) Consequences of asexuality in natural populations: insights from stick insects. Mol Biol Evol 35:1668–1677

    Article  CAS  Google Scholar 

  • Bast J, Jaron KS, Schuseil D, Roze D, Schwander T (2019) Asexual reproduction reduces transposable element load in experimental yeast populations. Elife 8:e48548

    Article  CAS  Google Scholar 

  • Begerow D, Bauer R, Boekhout T (2000) Phylogenetic placements of ustilaginomycetous anamorphs as deduced from nuclear LSU rDNA sequences. Mycol Res 104:53–60

    Article  CAS  Google Scholar 

  • Bell G (1982) The masterpiece of nature: the evolution and genetics of sexuality. California Press, Berkely

    Google Scholar 

  • Bell G (1988) Sex and death in protozoa: the history of an obsession. Cambridge University Press, Cambridge

    Google Scholar 

  • Bennett RJ, Turgeon BG (2016) Fungal sex: the ascomycota. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds) The fungal kingdom. American Society for Microbiology. https://doi.org/10.1128/microbiolspec.FUNK-0005-2016

  • Bernstein C, Bernstein H (1991) Aging, sex and DNA repair. Academic Press, San Diego

    Google Scholar 

  • Bernstein H, Byerly H, Hopf F, Michod RE (1988) Is meiotic recombination an adaptation for repairing DNA, producing genetic variation, or both? In: Michod RE, Levin BR (eds) The evolution of sex. Sinauer Ass Inc., Sunderland, pp 139–160

    Google Scholar 

  • Birdsell JA, Wills C (2003) The evolutionary origin and maintenance of sexual recombination: a review of contemporary models. In: Macintyre RJ, Clegg MT (eds) Evolutionary biology. Springer, Boston, pp 27–138

    Chapter  Google Scholar 

  • Birky CW Jr (1996) Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144:427–437

    Google Scholar 

  • Bleuyard JY, Gallego ME, White CI (2006) Recent advances in understanding of the DNA double-strand break repair machinery of plants. DNA Repair 5(1):1–12. https://doi.org/10.1016/j.dnarep.2005.08.017

    Article  CAS  Google Scholar 

  • Boenigk J, Wodniok S, Glücksman E (2015) Biodiversity and earth history. Springer, Berlin

    Book  Google Scholar 

  • Bouyer D, Kramdi A, Kassam M, Heese M, Schnittger A, Roudier F et al (2017) DNA methylation dynamics during early plant life. Genome Biol 18. https://doi.org/10.1186/s13059-017-1313-0

  • Brandeis M (2018) New-age ideas about age-old sex: separating meiosis from mating could solve a century-old conundrum. Biological Rev 93(2):801–810. https://doi.org/10.1111/brv.12367

    Article  Google Scholar 

  • Brandt A, Schaefer I, Glanz J, Schwander T, Maraun M, Scheu S et al (2017) Effective purifying selection in ancient asexual oribatid mites. Nat Commun 8:873

    Article  CAS  Google Scholar 

  • Brandt A, Bast J, Scheu S, Meusemann K, Donath A, Schütte K, Machida R, Kraaijeveld K (2019) No signal of deleterious mutation accumulation in conserved gene sequences of extant asexual hexapods. Sci Rep 9:5338

    Article  CAS  Google Scholar 

  • Brooks LA (1988) The evolution of recombination rates. In: Michod, RE, Levin, BR (eds) The evolution of sex. Sinauer, Sunderland

    Google Scholar 

  • Burki F, Roger AJ, Matthew W, Brown MW, Simpson AGB (2019) The new tree of eukaryotes. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2019.08.008

    Article  Google Scholar 

  • Burt A (2000) Perspective: sex, recombination, and the efficacy of selection—was Weismann right? Evolution 54(2):337–351

    CAS  Google Scholar 

  • Burt A, Carter DA, Koenig GL, White TJ, Taylor JW (1996) Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proc Nat Acad Sci USA 93(2):770–773

    Google Scholar 

  • Calkins GN (1919) Uroleptus mobilis Engelm. II. Renewal of vitality through conjugation. J Exp Zool 29:121–156

    Article  Google Scholar 

  • Castanera R, López-Varas L, Borgognone A, LaButti K, Lapidus A, Schmutz J et al (2016) Transposable elements versus the fungal genome: impact on whole-genome architecture and transcriptional profiles. PLOS Genet 12:e1006108

    Google Scholar 

  • Cavalier-Smith T (2010) Origin of the cell nucleus, mitosis and sex: roles of intracellular coevolution. Biol Direct 5:7

    Google Scholar 

  • Charlesworth D, Morgan M, Charlesworth B (1993a) Mutation accumulation in finite outbreeding and inbreeding populations. Genetics Res 61(01):39–56

    Google Scholar 

  • Charlesworth D, Morgan MT, Charlesworth B (1993b) Mutation accumulation in finite populations. J Hered 84:321–325

    Article  Google Scholar 

  • Chi J, Mahé F, Loidl J, Logsdon J, Dunthorn M (2014a) Meiosis gene inventory of four ciliates reveals the prevalence of a synaptonemal complex-independent crossover pathway. Mol Biol Evol 31:660–672

    Article  CAS  Google Scholar 

  • Chi J, Parrow MW, Dunthorn M (2014b) Cryptic sex in Symbiodinium (Alveolata, Dinoflagellata) is supported by an inventory of meiotic genes. J Eukaryot Microbiol 61:322–327

    Article  Google Scholar 

  • Coelho MA, Bakkeren G, Sun S, Hood ME, Giraud T (2017) Fungal sex: the Basidiomycota. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds) The fungal kingdom. American Society for Microbiology. https://doi.org/10.1128/microbiolspec.FUNK-0046-2016

  • Crow JF, Kimura M (1965) Evolution in sexual and asexual populations. Amer Naturalist 99:439–450

    Google Scholar 

  • Danchin EGJ, Rosso M-N, Vieira P, de Almeida-Engler J, Coutinho PM, Henrissat B, Abad P (2010) Multiple lateral gene transfers and duplications have promoted plant parasitism ability in nematodes. Proc Nat Acad Sci USA 107:17651–17656

    Article  CAS  Google Scholar 

  • Daskalov A, Heller J, Herzog S, Fleißner A, Glass NL (2017) Molecular mechanisms regulating cell fusion and heterokaryon formation in filamentous fungi. Microbiol Spectr 5:FUNK-0015-2016

    Google Scholar 

  • David-Palma M, Sampaio JP, Goncalves P (2016) Genetic dissection of sexual reproduction in a primary homothallic basidiomycete. PLoS Genet 12(6):e1006110. https://doi.org/10.1371/journal.pgen.1006110

  • de Visser JA, Elena SF (2007) The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 8:139–149

    Article  CAS  Google Scholar 

  • de Visser JA, Cooper TF, Elena SF (2011) The causes of epistasis. Proc Biol Sci 278:3617–3624

    Google Scholar 

  • Debortoli N, Li X, Eyres I, Fontaneto D, Hespeels B, Tang CQ et al (2016) Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Curr Biol 26:723–732

    Article  CAS  Google Scholar 

  • Doerder FP (2014) Abandoning sex: multiple origins of asexuality in the ciliate Tetrahymena. BMC Evol Biol 14:112

    Article  Google Scholar 

  • Dunthorn M, Katz LA (2010) Secretive ciliates and putative asexuality in microbial eukaryotes. Trends Microbiol 18:183–188

    Article  CAS  Google Scholar 

  • Dunthorn M, Stoeck T, Clamp J, Warren A, Mahé F (2014) Ciliates and the rare biopshere: a review. J Eukaryot Microbiol 61:404–409

    Article  Google Scholar 

  • Dunthorn M, Zufall RA, Chi J, Paszkiewicz K, Moore K, Mahé F (2017) Meiotic genes in colpodean ciliates support secretive sexuality. Genome Biol Evol 9:1781–1787

    Article  CAS  Google Scholar 

  • Dyer PS, Kück U (2017) Sex and the imperfect fungi. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY and Gow NAR (eds) The fungal kingdom. American Society for Microbiology, https://doi.org/10.1128/microbiolspec.FUNK-0043-2017

  • Eme L, Sharpe SC, Brown MW, Roger AJ (2014) On the age of eukaryotes: evaluating evidence from fossils and molecular clocks. Cold Spring Harb Perspect Biol 6:a016139

    Article  CAS  Google Scholar 

  • Engelstädter J (2017) Asexual but not clonal: evolutionary processes in automictic populations. Genetics 206:993–1009

    Article  Google Scholar 

  • Faddeeva-Vakhrusheva A, Kraaijeveld K, Derks MFL, Anvar SY, Agamennone V, Suring W et al (2017) Coping with living in the soil: the genome of the parthenogenetic springtail Folsomia candida. BMC Genomics 18:493

    Article  CAS  Google Scholar 

  • Felsenstein J (1974) The evolutionary advantage of recombination. Genetics 78:737–756

    CAS  Google Scholar 

  • Feng SH, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330(6004):622–627. https://doi.org/10.1126/science.1190614

    Article  CAS  Google Scholar 

  • Finlay BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296:1061–1063

    Article  CAS  Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Book  Google Scholar 

  • Flot J-F, Hespeels B, Li X, Noel B, Arkhipova I, Danchin EGJ, Hejnol A, Henrissat B, Koszul R, Aury J-M et al (2013) Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature 500:453–457

    Article  CAS  Google Scholar 

  • Flot JF, Debortoli N, Hallet B, Narayan J (2018) Reply to cross-contamination explains“ inter and intraspecific horizontal genetic transfers” between asexual bdelloid rotifers (Wilson, Nowell & Barraclough 2018) BioRxiv. https://www.biorxiv.org/content/10.1101/368209v1.abstract

  • Friedberg EC, Wlaker GC, Siede W, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2 edn. American Society for Microbiology, Washingtonn DC

    Google Scholar 

  • Gabriel W, Lynch M, Bürger R (1993) Muller’s ratchet and mutational meltdowns. Evolution 47:1744–1757

    Article  CAS  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma L-J, Wortman JR, Batzoglou S et al (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438(7071):1105–1115

    Google Scholar 

  • Gaston KJ, Blackburn TM, Lawton JH (1997) Interspecific abundance-range size relationships: an appraisal of mechanisms. J Anim Ecol 66:579–601

    Article  Google Scholar 

  • Gerstein AC, Otto SP (2009) Ploidy and the causes of genomic evolution. J Hered 100(5):571–581. https://doi.org/10.1093/jhered/esp057

    Article  CAS  Google Scholar 

  • Gladyshev E (2017) Repeat-induced point mutation and other genome defense mechanisms in fungi. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds) The fungal kingdom. American Society for Microbiology

    Google Scholar 

  • Glémin S, François CM, Galtier N (2019) Genome evolution in outcrossing vs. selfing vs. asexual species. Methods Mol Biol 1910:331–369

    Article  CAS  Google Scholar 

  • Glöckner G, Hülsmann N, Schleicher M, Noegel AA, Eichinger L, Gallinger C et al (2014) The genome of the foraminiferan Reticulomyxa filosa. Curr Biol 24:11–18. https://doi.org/10.1016/j.cub.2013.11.027

    Article  CAS  Google Scholar 

  • Golan JJ, Pringle A (2017) Long-distance dispersal of fungi. Microbiol Spectr 5:FUNK-0047-2016

    Google Scholar 

  • Gonçalves AP, Heller J, Span EA, Rosenfield G, Do HP, Palma-Guerrero J et al (2019) Allorecognition upon fungal cell-cell contact determines social cooperation and impacts the acquisition of multicellularity. Curr Biol 29:3006–3017

    Google Scholar 

  • Goodkov AV, Berdieva MA, Podlipaeva YI, Demin SYu (2019) The chromatin extrusion phenomenon in Amoeba proteus cell cycle. J Eukaryot Microbiol. https://doi.org/10.1111/jeu.12771

    Article  Google Scholar 

  • Gordo I, Charlesworth B (2000) The degeneration of asexual haploid populations and the speed of Muller’s ratchet. Genetics 154:1379–1387

    CAS  Google Scholar 

  • Green RF, Noakes DLG (1995) Is a little bit of sex as good as a lot? J Theor Biol 174(1):87–96. https://doi.org/10.1006/jtbi.1995.0081

    Article  Google Scholar 

  • Grusz AL (2016) A current perspective on apomixis in ferns. J Syst Evol 54(6):656–665. https://doi.org/10.1111/jse.12228

    Article  Google Scholar 

  • Halary S, Malik SB, Lildhar L, Slamovits CH, Hijri M, Corradi N (2011) Conserved meiotic machinery in Glomus spp., a putatively ancient asexual fungal lineage. Genome Biol Evol 3:950–958

    Google Scholar 

  • Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35:282–290

    Article  Google Scholar 

  • Hand ML, Koltunow AMG (2014) The genetic control of apomixis: asexual seed formation. Genetics 197(2):441–450. https://doi.org/10.1534/genetics.114.163105

    Article  CAS  Google Scholar 

  • Hartfield M (2016) Evolutionary genetic consequences of facultative sex and outcrossing. J Evol Biol 29:5–22

    Article  CAS  Google Scholar 

  • Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spectr 5:FUNK-0052-2016

    Google Scholar 

  • Heitman J (2015) Evolution of sexual reproduction: a view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol Reviews 29:108–117

    Article  Google Scholar 

  • Hickey DA (1992) Evolutionary dynamics of transposable elements in prokaryotes and eukaryotes. Genetica 86:269–274

    Article  CAS  Google Scholar 

  • Hill WG, Robertson A (1966) The effect of linkage on limits to artificial selection. Genet Res 8:269–294

    Article  CAS  Google Scholar 

  • Hodac L, Klatt S, Hojsgaard D, Sharbel T, Hörandl E (2019) A little bit of sex prevents mutation accumulation even in apomictic polyploid plants. BMC Evol Biol 19:170. https://doi.org/10.1186/s12862-019-1495-z

    Article  CAS  Google Scholar 

  • Hofstatter PG, Lahr DJG (2019) All eukaryotes are sexual, unless proven otherwise. BioEssays 41:e1800246. https://doi.org/10.1002/bies.201800246

    Article  Google Scholar 

  • Hofstatter PG, Brown MW, Lahr DJG (2018) Comparative genomics supports sex and meiosis in diverse Amoebozoa. Mol Biol Evol 10:3118–3128. https://doi.org/10.1093/gbe/evy241

    Article  CAS  Google Scholar 

  • Hojsgaard D, Hörandl E (2019) The rise of apomixis in natural plant populations. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00358

  • Hojsgaard D, Klatt S, Baier R, Carman JG, Hörandl E (2014) Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. Crit Rev Plant Sci 33(5):414–427. https://doi.org/10.1080/07352689.2014.898488

    Article  Google Scholar 

  • Holliday R (1984) The biological significance of meiosis. Symposia Soc ExperBiol 38:381–394

    CAS  Google Scholar 

  • Hollister JD, Greiner S, Wang W, Wang J, Zhang Y, Wong GK-S et al (2015) Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera. Mol Biol Evol 32(4):896–905

    Google Scholar 

  • Hörandl E (2009) A combinational theory for maintenance of sex. Heredity 103(6):445–457. https://doi.org/10.1038/hdy.2009.85

    Article  Google Scholar 

  • Hörandl E (2010) The evolution of self-fertility in apomictic plants. Sex Pl Repr 23(1):73–86. https://doi.org/10.1007/s00497-009-0122-3

    Article  Google Scholar 

  • Hörandl E, Hadacek F (2013) The oxidative damage initiation hypothesis for meiosis. Sex Pl Repr 26:351–367

    Article  CAS  Google Scholar 

  • Hörandl E, Hadacek F (2020) Oxygen, life forms, and the evolution of sexes in multicellular eukaryotes. Heredity (in press). https://doi.org/10.1038/s41437-020-0317-9

  • Hörandl E, Speijer D (2018) How oxygen gave rise to eukaryotic sex. Proc B-Biol Sci 285(1872):20172706. https://doi.org/10.1098/rspb.2017.2706

    Article  CAS  Google Scholar 

  • Ibarra CA, Feng XQ, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA et al (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337(6100):1360–1364. https://doi.org/10.1126/science.1224839

    Article  CAS  Google Scholar 

  • Jaenike J (1978) An hypothesis to account for the maintenance of sex within populations. Evol Theory 3:191–194

    Google Scholar 

  • Jain K (2008) Loss of least-loaded class in asexual populations due to drift and epistasis. Genetics 179(4):2125–2134

    Google Scholar 

  • Jalvingh K, Bast J, Schwander T (2016) Sex, evolution and maintenance of. Encyclopedia of evolutionary biology [Internet], pp 89–97. Available from: https://doi.org/10.1016/b978-0-12-800049-6.00144-x

  • Jaron KS, Bast J, Nowell RW, Rhyker Ranallo-Benavidez T, Robinson-Rechavi M, Schwander T (2019) Genomic features of asexual animals. bioRxiv [Internet], p 497495. Available from: https://www.biorxiv.org/content/10.1101/497495v2

  • Jiang X, Tang H, Ye Z, Lynch M (2017) Insertion polymorphisms of mobile genetic elements in sexual and asexual populations of Daphnia pulex. Genome Biol Evol 9:362–374

    CAS  Google Scholar 

  • Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97–100

    Article  CAS  Google Scholar 

  • Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N et al (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. Plos Genetics 5(6). https://doi.org/10.1371/journal.pgen.1000530

  • Judson OP, Normark BB (1996) Ancient asexual scandals. Trends Ecol Evol 11:41–46

    Article  CAS  Google Scholar 

  • Kantama L, Sharbel TF, Schranz ME, Mitchell-Olds T, de Vries S, de Jong H (2007) Diploid apomicts of the Boechera holboellii complex display large-scale chromosome substitutions and aberrant chromosomes. Proc Nat Acad Sci USA 104(35):14026–14031. https://doi.org/10.1073/pnas.0706647104

    Article  CAS  Google Scholar 

  • Katz LA (2001) Evolution of nuclear dualism in ciliates: a reanalysis in light of recent molecular data. Int J Syst Evol Microbiol 51:1587–1592

    Article  CAS  Google Scholar 

  • Keeling P, Burki F (2019) Progress towards the tree of eukaryotes. Curr Biol 29:R808–R817

    Article  CAS  Google Scholar 

  • Keightley PD, Otto SP (2006) Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443:89–92

    Article  CAS  Google Scholar 

  • Kiefer M, Nauerth BH, Volkert C, Ibberson D, Loreth A, Schmidt A (2020) Gene function rather than reproductive mode drives the evolution of RNA helicases in sexual and apomictic Boechera. Genome Biol Evol https://doi.org/10.1093/gbe/evaa078

  • Klatt S, Hadacek F, Hodač L, Brinkmann G, Eilerts M, Hojsgaard D et al (2016) Photoperiod extension enhances sexual megaspore formation and triggers metabolic reprogramming in facultative apomictic Ranunculus auricomus. Front Plant Sci 7:278. https://doi.org/10.3389/fpls.2016.00278

    Article  Google Scholar 

  • Klatt S, Schinkel CC, Kirchheimer B, Dullinger S, Hörandl E (2018) Effects of cold treatments on fitness and mode of reproduction in the diploid and polyploid alpine plant Ranunculus kuepferi (Ranunculaceae) Ann Bot 121(7):1287–1298

    Google Scholar 

  • Kliver S, Rayko M, Komissarov A, Bakin E, Zhernakova D, Prasad K et al (2018) Assembly of the Boechera retrofracta genome and evolutionary analysis of apomixis-associated genes. Genes 9(4):16. https://doi.org/10.3390/genes9040185

    Article  CAS  Google Scholar 

  • Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Ann Rev Plant Biol 54:547–574. https://doi.org/10.1146/annurev.arplant.54.110901.160842

    Article  CAS  Google Scholar 

  • Kondrashov AS (1988) Deleterious mutations and the evolution of sexual reproduction. Nature 336(6198):435–440. https://doi.org/10.1038/336435a0

    Article  CAS  Google Scholar 

  • Kondrashov AS (1993) Classification of hypotheses on the advantage of amphimixis. J Hered 84:372–387

    Article  CAS  Google Scholar 

  • Kondrashov AS, Crow JF (1991) Haploidy or diploidy: which is better? Nature 351(6324):314–315

    Article  CAS  Google Scholar 

  • Koonin EV, Makarova KS, Wolf YI, Krupovic M (2020) Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire. Nat Rev Genet 21:119–131

    Article  CAS  Google Scholar 

  • Kouyos RD, Silander OK, Bonhoeffer S (2007) Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol 22(6):308–315

    Google Scholar 

  • Kraaijeveld K, Anvar SY, Frank J, Schmitz A, Bast J, Wilbrandt J et al (2016) Decay of sexual trait genes in an asexual parasitoid wasp. Genome Biol Evol 8:3685–3695

    CAS  Google Scholar 

  • Kraus D, Chi J, Boenigk J, Beisser D, Graupner N, Dunthorn M (2018) Putatively asexual chrysophytes have meiotic genes: evidence from transcriptomic data. Peer J 6:e5894

    Article  CAS  Google Scholar 

  • Kües U, James TY, Heitman J (2011) Mating type in basidiomycetes: unipolar, bipolar, and tetrapolar patterns of sexuality. In: Pöggeler S, Wöstemeyer J (eds) The Mycota XIV. Evolution of fungi and fungal-like organisms. Springer, Berlin, pp 97–160

    Google Scholar 

  • Laine V, Sackton T, Meselson M (2020) Sexual reproduction in bdelloid rotifers. bioRxiv. https://doi.org/10.1101/2020.08.06.23959

  • Lanfranco L, Bonfante P, Genre A (2016) The mutualistic interaction between plants and arbuscular mycorrhizal fungi. Microbiol Spectr 4:FUNK-0012-2016

    Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11(3):204–220. https://doi.org/10.1038/nrg2719

    Article  CAS  Google Scholar 

  • Lee SC, Idnurm A (2017) Fungal sex: the Mucoromycota. In: Heitman J, Howlett BJ, Crous PW, Stukenbrock EH, James TY, Gow NAR (eds) The fungal kingdom. American Society for Microbiology. https://doi.org/10.1128/microbiolspec.FUNK-0041-2017

  • Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA, Graham SW et al (2019) One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574(7780):679. https://doi.org/10.1038/s41586-019-1693-2

  • Leria L, Vila-Farré M, Solà E, Riutort M (2019) Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex. BMC Evol Biol 19:130

    Article  Google Scholar 

  • Lewis WM (1987) The cost of sex. In: Stearns SC (ed) The evolution of sex and its consequences. Birkhäuser, Basel, pp 33–57

    Chapter  Google Scholar 

  • Lin X, Hull CM, Heitman J (2005) Sexual reproduction between partners of the same mating type in Cryptococcus neoformans. Nature 434(7036):1017–1021. https://doi.org/10.1038/nature03448

  • Lin X, Heitman J (2007) Mechanisms of homothallism in fungi and transitions between heterothallism and homothallism, pp 35–57. In: Heitman J, Kronstad JW, Taylor JW, Casselton LA (eds) Sex in fungi: molecular determination and evolutionary implications. ASM Press, Washington, DC. https://doi.org/10.1128/9781555815837.ch3

  • Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DGO, Mu D et al (2014) Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLOS Genet 10(1):e1004078. https://doi.org/10.1371/journal.pgen.1004078

    Article  CAS  Google Scholar 

  • Lindsey ARI, Kelkar YD, Wu X, Sun D, Martinson EO, Yan Z, Rugman-Jones PF, Hughes DST, Murali SC, Qu J, Dugan S, Lee SL, Chao H, Dinh H, Han Y, Doddapaneni HV, Worley KC, Muzny DM, Ye G, Gibbs RA, Richards S, Yi SV, Stouthamer R, Werren JH (2018) Comparative genomics of the miniature wasp and pest control agent Trichogramma pretiosum. BMC Biol 16:54

    Article  CAS  Google Scholar 

  • Logares R, Audic S, Bass D, Bittner L, Boutte C, Christen R et al (2014) Patterns of rare and abundant marine microbial eukaryotes. Curr Biol 24:813–821

    Article  CAS  Google Scholar 

  • Lovell JT, Williamson RJ, Wright SI, McKay JK, Sharbel TF (2017) Mutation accumulation in an asexual relative of arabidopsis. Plos Genet 13(1). https://doi.org/10.1371/journal.pgen.1006550

  • Lunt DH (2008) Genetic tests of ancient asexuality in root knot nematodes reveal recent hybrid origins. BMC Evol Biol 8:194

    Article  CAS  Google Scholar 

  • Lynch M (2007) The origins of genome architecture. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Lynch M, Bürger R, Butcher D, Gabriel W (1993) The mutational meltdown in asexual populations. J Hered 84:339–344

    Article  CAS  Google Scholar 

  • Lynn DH (2008) The ciliated protozoa: characterization, classification, and guide to the literature, 3rd edn. Springer, Dordrecht

    Google Scholar 

  • Maciver SK (2016) Asexual amoebae escape Muller’s ratchet through polyploidy. Trends Parasitol 32:855–862. https://doi.org/10.1016/j.pt.2016.08.006

    Article  Google Scholar 

  • Maheshwari R (2005) Nuclear behavior in fungal hyphae. FEMS Microbiol Lett 249:7–14. https://doi.org/10.1016/j.femsle.2005.06.031

    Article  CAS  Google Scholar 

  • Malik S-B, Pightling AW, Stefaniak LM, Schurko AM, Logsdon JM (2008) An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3:e2879

    Article  Google Scholar 

  • Marais G (2003) Biased gene conversion: implications for genome and sex evolution. Trends Genet 19:330–338

    Article  CAS  Google Scholar 

  • Maraun M, Norton RA, Ehnes RB, Scheu S, Erdmann G (2012) Positive correlation between density and parthenogenetic reproduction in oribatid mites (Acari) supports the structured resource theory of sexual reproduction. Evol Ecol Res 14:311–323

    Google Scholar 

  • Mark Welch DB, Meselson M (2000) Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288:1211–1215

    Article  CAS  Google Scholar 

  • Mark Welch DB, Mark Welch JL, Meselson M (2008) Evidence for degenerate tetraploidy in bdelloid rotifers. Proc Natl Acad Sci USA 105:5145–5149

    Article  Google Scholar 

  • Maron JL, Johnson MTJ, Hastings AP, Agrawal AA (2018) Fitness consequences of occasional outcrossing in a functionally asexual plant (Oenothera biennis). Ecology 99(2):464–473. https://doi.org/10.1002/ecy.2099

  • Martinez G, Panda K, Kohler C, Slotkin RK (2016) Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nat Plants 2(4). https://doi.org/10.1038/nplants.2016.30

  • Matzke MA, Kanno T, Matzke AJM (2015) RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. In: Merchant SS (ed) Annual review of plant biology, vol 66, pp 243–267

    Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge

    Google Scholar 

  • Michael TP (2014) Plant genome size variation: bloating and purging DNA. Brief Funct Genom 13(4):308–317

    Article  CAS  Google Scholar 

  • Mirzaghaderi G, Hörandl E (2016) The evolution of meiotic sex and its alternatives. Proc B-Biol Sci 283(1838). https://doi.org/10.1098/rspb.2016.1221

  • Mogie M (1992) The evolution of asexual reproduction in plants. Chapman and Hall, London

    Google Scholar 

  • Morgens DW, Cavalcanti ARO (2015) Amitotic chromosome loss predicts distinct patterns of senescence and non-senescence in ciliates. Protist 166:224–233. https://doi.org/10.1016/j.protis.2015.03.002

    Article  Google Scholar 

  • Morrow CA, Fraser JA (2009) Sexual reproduction and dimorphism in the pathogenic basidiomycetes. FEMS Yeast Res 9:161–177. https://doi.org/10.1111/j.1567-1364.2008.00475.x

    Article  CAS  Google Scholar 

  • Muller HJ (1932) Some genetic aspects of sex. Am Nat 66:118–138

    Google Scholar 

  • Muller HJ (1964) The relation of recombination to mutational advance. Mutation research 106:2–9

    Google Scholar 

  • Neiman M, Sharbel TF, Schwander T (2014) Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. J Evol Biol 27:1346–1359

    Article  CAS  Google Scholar 

  • Neiman M, Lively CM, Meirmans S (2017) Why sex? A pluralist approach revisited. Trends Ecol Evol 32(8):589–600. https://doi.org/10.1016/j.tree.2017.05.004

    Article  Google Scholar 

  • Neiman M, Meirmans PG, Schwander T, Meirmans S (2018) Sex in the wild: how and why field-based studies contribute to solving the problem of sex. Evolution 72(6):1194–1203. https://doi.org/10.1111/evo.13485

    Article  Google Scholar 

  • Ni M, Feretzaki M, Li W, Floyd-Averette A, Mieczkowski P, Dietrich FS, Heitman J (2013) Unisexual and heterosexual meiotic reproduction generate aneuploidy and phenotypic diversity de novo in the yeast Cryptococcus neoformans. PLoS Biol 11(9):e1001653. https://doi.org/10.1371/journal.pbio.1001653

  • Normark BB (1999) Evolution in a putatively ancient asexual aphid lineage: recombination and rapid karyotype change. Evolution [Internet] 53:1458. Available from: https://doi.org/10.2307/2640892

  • Normark BB, Johnson NA (2011) Niche explosion. Genetica 139:551–564

    Article  Google Scholar 

  • Normark BB, Judson OP, Moran NA (2003) Genomic signatures of ancient asexual lineages. Biol J Linn Soc Lond 79:69–84

    Article  Google Scholar 

  • Nowell RW, Almeida P, Wilson CG, Smith TP, Fontaneto D, Crisp A et al (2018) Comparative genomics of bdelloid rotifers: insights from desiccating and nondesiccating species. PLOS Biol [Internet] 16:e2004830. Available from: https://doi.org/10.1371/journal.pbio.2004830

  • Oberwinkler F (2017) Yeasts in pucciniomycotina. Mycol Prog 16:831–856. https://doi.org/10.1007/s11557-017-1327-8

  • O’Gorman CM, Fuller HT, Dyer PS (2009) Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471–475

    Article  CAS  Google Scholar 

  • Ollivier M, Gabaldón T, Poulain J, Gavory F, Leterme N, Gauthier J-P, Legeai F, Tagu D, Simon JC, Rispe C (2012) Comparison of gene repertoires and patterns of evolutionary rates in eight aphid species that differ by reproductive mode. Genome Biol Evol 4:155–167

    Article  CAS  Google Scholar 

  • Ong-Abdullah M, Ordway JM, Jiang N, Ooi SE, Kok SY, Sarpan N et al (2015) Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature 525(7570):533. https://doi.org/10.1038/nature15365

  • Otto SP (2009) The evolutionary enigma of sex. Am Nat 174:S1–S14. https://doi.org/10.1086/599084

    Article  Google Scholar 

  • Ozias-Akins P, Conner JA (2019) Clonal reproduction through seeds in sight for crops. Trends Genet (in press). https://doi.org/10.1016/j.tig.2019.12.006

  • Ozias-Akins P, van Dijk PJ (2007) Mendelian genetics of apomixis in plants. Ann Rev Genet 41:509–537. https://doi.org/10.1146/annurev.genet.40.110405.09051

    Article  CAS  Google Scholar 

  • Parfrey LW, Lahr DJG, Katz LA (2008) The dynamic nature of eukaryotic genomes. Mol Biol Evol 25:787–794. https://doi.org/10.1093/molbev/msn032

    Article  CAS  Google Scholar 

  • Parker DJ, Bast J, Jalvingh K, Dumas Z, Robinson-Rechavi M, Schwander T (2019) Repeated evolution of asexuality involves convergent gene expression changes. Mol Biol Evol 36:350–364

    Article  CAS  Google Scholar 

  • Pellino M, Hojsgaard D, Schmutzer T, Scholz U, Hörandl E, Vogel H et al (2013) Asexual genome evolution in the apomictic Ranunculus auricomus complex: examining the effects of hybridization and mutation accumulation. Molec Ecol 22(23):5908–5921. https://doi.org/10.1111/mec.12533

    Article  CAS  Google Scholar 

  • Peraza-Reyes L, Malagnac F (2016) Sexual development in fungi. In: Wendland J (ed) The Mycota I, 3rd edn. Springer, Berlin

    Google Scholar 

  • Pöggeler S (2002) Genomic evidence for mating abilities in the asexual pathogen Aspergillus fumigatus. Curr Genet 42(3):153–160

    Google Scholar 

  • Pöggeler S, Nowrousian M, Teichert I, Beier A, Kück U (2018) Fruiting body development in ascomycetes. In: Anke T, Schüffler A (eds) The Mycota XV, physiology and genetics, 2nd edn. Springer, Berlin

    Google Scholar 

  • Raikov IB (1982) The protozoan nucleus: morphology and evolution. Springer, Wien

    Google Scholar 

  • Ramesh MA, Malik S-B, Logsdon JM (2005) A phylogenomic inventory of meiotic genes: evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr Biol 15(2):185–191

    Google Scholar 

  • Raudaskoski M, Kothe E (2010) Basidiomycete mating type genes and pheromone signaling. Eukaryot Cell 9:847–859. https://doi.org/10.1128/EC.00319-09.

  • Rice WR, Friberg U (2009) A graphical approach to lineage selection between clonals and sexuals. In: Schön I, Martens K, Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer, Dordrecht, pp 75–97

    Google Scholar 

  • Richards CL, Alonso C, Becker C, Bossdorf O, Bucher E, Colome-Tatche M et al (2017) Ecological plant epigenetics: evidence from model and non-model species, and the way forward. Ecol Lett 20(12):1576–1590. https://doi.org/10.1111/ele.12858

    Article  Google Scholar 

  • Ropars J, Toro KS, Noel J, Pelin A, Charron P, Farinelli L et al (2016) Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi. Nat Microbiol 1(6):16033. https://doi.org/10.1038/nmicrobiol.2016.33

    Article  CAS  Google Scholar 

  • Ross L, Hardy NB, Okusu A, Normark BB (2013) Large population size predicts the distribution of asexuality in scale insects. Evolution 67:196–206

    Article  Google Scholar 

  • Sampaio JP (2004) Diversity, phylogeny and classification of basidiomycetous yeasts. In: Agerer R, Piepenbring M, Blanz P (eds) Frontiers in basidiomycote mycology. IHW, Eching, pp 49–80

    Google Scholar 

  • Saunders CW, Scheynius A, Heitman J (2012) Malassezia fungi are specialized to live on skin and associated with dandruff, eczema, and other skin diseases. PLoS Pathog 8(6):e1002701. https://doi.org/10.1371/journal.ppat.1002701

    Article  CAS  Google Scholar 

  • Schemske DW, Lande R (1985) The evolution of self-fertilization and inbreeding depression in plants. II. Empirical observations. Evolution 39:41–52

    Article  Google Scholar 

  • Scheu S, Drossel B (2007) Sexual reproduction prevails in a world of structured resources in short supply. Proc R Soc B-Biol Sci 274:1225–1231

    Article  CAS  Google Scholar 

  • Schmidt A, Schmid MW, Klostermeier UC, Qi WH, Guthorl D, Sailer C et al (2014) Apomictic and sexual germline development differ with respect to cell cycle, transcriptional, hormonal and epigenetic regulation. PLoS Genet 10(7):21. https://doi.org/10.1371/journal.pgen.1004476

    Article  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  CAS  Google Scholar 

  • Schön I, Martens K (2003) No slave to sex. Proc B-Biol Sci 270:827–833

    Article  Google Scholar 

  • Schön I, Martens K, van Dijk P (2009) Lost sex: the evolutionary biology of parthenogenesis. Springer, Berlin

    Book  Google Scholar 

  • Schurko AM, Logsdon JM (2008) Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. BioEssays 30(6):579–589. https://doi.org/10.1002/bies.20764

    Article  CAS  Google Scholar 

  • Schurko AM, Neiman M, Logsdon JM (2009) Signs of sex: what we know and how we know it. Trends Ecol Evol 24:208–217

    Article  Google Scholar 

  • Schwander T (2016) Evolution: the end of an ancient asexual scandal. Curr Biol 26:R233–R235

    Article  CAS  Google Scholar 

  • Schwander T, Crespi BJ (2009a) Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Molec Ecol 18(1):28–42. https://doi.org/10.1111/j.1365-294X.2008.03992.x

    Article  Google Scholar 

  • Schwander T, Crespi BJ (2009b) Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Mol Ecol 18:28–42

    Article  Google Scholar 

  • Schwander T, Henry L, Crespi BJ (2011) Molecular evidence for ancient asexuality in timema stick insects. Curr Biol 21:1129–1134

    Article  CAS  Google Scholar 

  • Sharbel TF, Voigt M-L, Corral JM, Galla G, Kumlehn J, Klukas C et al (2010) Apomictic and sexual ovules of boechera display heterochronic global gene expression patterns. Plant Cell 22(3):655–671. https://doi.org/10.1105/tpc.109.072223

    Article  CAS  Google Scholar 

  • Sharp NP, Otto SP (2016) Evolution of sex: Using experimental genomics to select among competing theories. BioEssays 38:751–757

    Article  Google Scholar 

  • Shiu PKT, Raju NB, Zickler D, Metzenberg RL (2001) Meiotic silencing by unpaired DNA. Cell 107(7):905–916

    Google Scholar 

  • Signorovitch A, Hur J, Gladyshev E, Meselson M (2015) Allele sharing and evidence for sexuality in a mitochondrial clade of bdelloid rotifers. Genetics 200:1–10

    Article  CAS  Google Scholar 

  • Simon JC, Delmotte F, Rispe C, Crease T (2003) Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biol J Linn Soc 79:151–163

    Article  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  CAS  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in Pollen. Cell 136(3):461–472. https://doi.org/10.1016/j.cell.2008.12.038

    Article  CAS  Google Scholar 

  • Song Y, Drossel B, Scheu S (2011) Tangled bank dismissed too early. Oikos 120:1601–1607

    Article  Google Scholar 

  • Spatafora JW, Aime MC, Grigoriev IV, Martin F, Stajich JE, Blackwell M (2017) The fungal tree of life: from molecular systematics to genome-scale phylogenies. Microbiol Spectr 5:FUNK-0053-2016

    Google Scholar 

  • Speijer D (2016) What can we infer about the origin of sex in early eukaryotes? Philos Trans Roy Soc B-Biol Sci 371(1706). https://doi.org/10.1098/rstb.2015.0530

  • Speijer D, Lukes J, Elias M (2015) Sex is a ubiquitous, ancient, and inherent attribute of eukaryotic life. Proc Natl Acad Sci USA 112(29):8827–8834. https://doi.org/10.1073/pnas.1501725112

    Article  CAS  Google Scholar 

  • Stajich JE (2017) Fungal genomes and insights into the evolution of the kngdom. Microbiol Spectr 5.https://doi.org/10.1128/microbiolspec.FUNK-0055-2016

  • Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press

    Google Scholar 

  • Szitenberg A, Cha S, Opperman CH, Bird DM, Blaxter ML, Lunt DH (2016) Genetic drift, not life history or RNAi, determine long-term evolution of transposable elements. Genome Biol Evol 8:2964–2978

    Article  CAS  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R et al (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Nat Acad Sci USA 110(50):20117–20122. https://doi.org/10.1073/pnas.1313452110

    Article  CAS  Google Scholar 

  • Tucker AE, Ackerman MS, Eads BD, Xu S, Lynch M (2013) Population-genomic insights into the evolutionary origin and fate of obligately asexual Daphnia pulex. Proc Natl Acad Sci USA 110:15740–15745

    Article  CAS  Google Scholar 

  • Ulum FB, Costa Castro C, Hörandl E (2020) Ploidy-dependent effects of light stress on the mode of reproduction in the Ranunculus auricomus complex (Ranunculaceae). Front Plant Sci 11:104. https://doi.org/10.3389/fpls.2020.00104

  • Vakhrusheva OA, Mnatsakanova EA, Galimov YR, Neretina TV, Gerasimov ES, Ozerova SG et al (2018) Recombination in a natural population of the bdelloid rotifer Adineta vaga. bioRxiv [Internet]:489393. Available from: https://www.biorxiv.org/content/early/2018/12/17/489393

  • van der Kooi CJ, Matthey-Doret C, Schwander T (2017) Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evol Lett 1:304–316

    Article  Google Scholar 

  • Verhoeven KJF, Preite V (2014) Epigenetic variation in asexually reproducing organisms. Evolution 68(3):644–655. https://doi.org/10.1111/evo.12320

    Article  Google Scholar 

  • Vos M, Hesselman MC, te Beek TA, van Passel MWJ, Eyre-Walker A (2015) Rates of lateral gene transfer in prokaryotes: high but why? Trends Microbiol 23(10):598–605. https://doi.org/10.1016/j.tim.2015.07.006

    Article  CAS  Google Scholar 

  • Wang QM, Begerow D, Groenewald M, Liu XZ, Theelen B, Bai FY, Boekhout T (2015) Multigene phylogeny and taxonomic revision of yeasts and related fungi in the Ustilaginomycotina. Stud Mycol 81:55–83. https://doi.org/10.1016/j.simyco.2015.10.004

    Article  Google Scholar 

  • Wang X, Xu YT, Zhang SQ, Cao L, Huang Y, Cheng JF et al (2017) Genomic analyses of primitive, wild and cultivated Citrus provide insights into asexual reproduction. Nature Genet 49(5):765. https://doi.org/10.1038/ng.3839

  • Warren WC, García-Pérez R, Xu S, Lampert KP, Chalopin D, Stöck M, Loewe L, Lu Y, Kuderna L, Minx P, Montague MJ, Tomlinson C, Hillier LW, Murphy DN, Wang J, Wang Z, Garcia CM, Thomas GCW, Volff J-N, Farias F, Aken B, Walter RB, Pruitt KD, Marques-Bonet T, Hahn MW, Kneitz S, Lynch M, Schartl M (2018) Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nat Ecol Evol 2:669–679

    Article  Google Scholar 

  • Watts PC, Lundholm N, Ribeiro S, Ellegaard M (2013) A century-long genetic record reveals that protist effective population sizes are comparable to those of macroscopic species. Biol Lett 9:20130849. https://doi.org/10.1098/rsbl.2013.0849

    Article  Google Scholar 

  • Weismann A (1904) The evolution theory. Edward Arnold, London

    Book  Google Scholar 

  • Weisse T, Anderson R, Arndt H, Calbet A, Hansen PJ, Montagnes DJS (2016) Functional ecology of aquatic phagotrophic protists—concepts, limitations, and perspectives. Eur J Protistol 55:50–74. https://doi.org/10.1016/j.ejop.2016.03.003

    Article  Google Scholar 

  • Wendte JM, Zhang YW, Ji LX, Shi XL, Hazarika RR, Shahryary Y et al (2019) Epimutations are associated with CHROMOMETHYLASE 3-induced de novo DNA methylation. Elife 8. https://doi.org/10.7554/eLife.47891

  • West SA, Lively CM, Read AF (1999) A pluralist approach to sex and recombination. J Evol Biol 12:1003–1012

    Article  Google Scholar 

  • White MJD (1977) Animal cytology and evolution. CUP Archive

    Google Scholar 

  • White EP, Ernest SKM, Kerkhoff AJ, Enquist BJ (2007) Relationships between body size and abundance in ecology. Trends Ecol Evol 22:323–330

    Article  Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton

    Google Scholar 

  • Wilson CG, Nowell RW, Barraclough TG (2018) Cross-contamination explains “inter and intraspecific horizontal genetic transfers” between asexual bdelloid rotifers. Curr Biol 28:2436-2444.e14

    Article  CAS  Google Scholar 

  • Wright S, Finnegan D (2001) Genome evolution: sex and the transposable element. Curr Biol 11(8):R296–R299. https://doi.org/10.1016/s0960-9822(01)00168-3

    Article  CAS  Google Scholar 

  • Zhang H, West JA, Zufall RA, Azevedo RBR (2019) Amitosis confers benefits of sex in the absence of sex to Tetrahymena. bioRxiv 794735

    Google Scholar 

  • Zhao Y, Wang Y, Upadhyay S, Xue C, Lin X (2020) Activation of meiotic genes mediates ploidy reduction during cryptococcal infection. Curr Biol 30:1387-1396.e5. https://doi.org/10.1016/j.cub.2020.01.081

    Article  CAS  Google Scholar 

  • Zickler D, Espagne E (2016) Sordaria, a model system to uncover links between meiotic pairing and recombination. Semin Cell Dev Biol 54:149–157

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the editors, Marie-Hélène Rome and Pierre Pontarotti, for inviting us to contribute to this book, and one anonymous referee for valuable comments on the manuscript. The work on this chapter was supported by Deutsche Forschungsgemeinschaft (DFG), projects 4395/4-1 and 4395/10-1 to E.H., BA 5800/3-1 to J.B., DU1319/5-1 to M.D., NO407/7-1 to M.N.

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Hörandl, E. et al. (2020). Genome Evolution of Asexual Organisms and the Paradox of Sex in Eukaryotes. In: Pontarotti, P. (eds) Evolutionary Biology—A Transdisciplinary Approach. Springer, Cham. https://doi.org/10.1007/978-3-030-57246-4_7

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