Sexual reproduction is the primary mode of reproduction in eukaryotes, but some organisms have evolved deviations from classical sex and switched to asexuality. These asexual lineages have sometimes been viewed as evolutionary dead ends, but recent research has revealed their importance in many areas of general biology. Our review explores the understudied, yet important mechanisms by which sperm-dependent asexuals that produce non-recombined gametes but rely on their fertilization, can have a significant impact on the evolution of coexisting sexual species and ecosystems. These impacts are concentrated around three major fields. Firstly, sperm-dependent asexuals can potentially impact the gene pool of coexisting sexual species by either restricting their population sizes or by providing bridges for interspecific gene flow whose type and consequences substantially differ from gene flow mechanisms expected under sexual reproduction. Secondly, they may impact on sexuals' diversification rates either directly, by serving as stepping-stones in speciation, or indirectly, by promoting the formation of pre- and postzygotic reproduction barriers among nascent species. Thirdly, they can potentially impact on spatial distribution of species, via direct or indirect (apparent) types of competition and Allee effects. For each such mechanism, we provide empirical examples of how natural sperm-dependent asexuals impact the evolution of their sexual counterparts. In particular, we highlight that these broad effects may last beyond the tenure of the individual asexual lineages causing them, which challenges the traditional perception that asexual lineages are short-lived evolutionary dead ends and minor sideshows. Our review also proposes new research directions to incorporate the aforementioned impacts of sperm-dependent asexuals. These research directions will ultimately enhance our understanding of the evolution of genomes and biological interactions in general.

Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czech Republic

Department of Biology International Stock Center for Livebearing Fishes Oklahoma Norman USA

Department of Biology University of Oklahoma Oklahoma Norman USA

Department of Plant Developmental Genetics Institute of Biophysics Academy of Sciences of the Czech Republic Brno Czech Republic

Department of Zoology Faculty of Natural Sciences Comenius University in Bratislava Bratislava Slovakia

Laboratory of Non Mendelian Evolution Institute of Animal Physiology and Genetics Academy of Sciences of the Czech Republic Liběchov Czech Republic

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Alves, M. J. , Coelho, M. M. , & Collares‐Pereira, M. J. (2001). Evolution in action through hybridisation and polyploidy in an Iberian freshwater fish: A genetic review. Genetica, 111, 375–385. PubMed

Alves, M. J. , Collares‐Pereira, M. J. , Dowling, T. E. , & Coelho, M. M. (2002). The genetics of maintenance of an all‐male lineage in the Squalius alburnoides complex. Journal of Fish Biology, 60, 649–662.

Amundsen, T. (2018). Sex roles and sexual selection: Lessons from a dynamic model system. Current Zoology, 64, 363–392. PubMed PMC

Angers, B. , Leung, C. , Vétil, R. , Deremiens, L. , & Vergilino, R. (2018). The effects of allospecific mitochondrial genome on the fitness of northern redbelly dace (Chrosomus eos). Ecology and Evolution, 8, 3311–3321. PubMed PMC

Angers, B. , & Schlosser, I. J. (2007). The origin of Phoxinus eos‐neogaeus unisexual hybrids. Molecular Ecology, 16, 4562–4571. PubMed

Arano, B. , Llorente, G. A. , Herrero, P. , & Sanchiz, B. (1994). Current studies on Iberian water frogs. Zoologica Poloniae, 39, 365–375.

Avise, I. J. (2008). Clonality: The genetics, ecology, and evolution of sexual abstinence in vertebrate animals: The genetics, ecology, and evolution of sexual abstinence in vertebrate animals. University of California. Oxford University Press.

Barbuti, R. , Mautner, S. , Carnevale, G. , Milazzo, P. , Rama, A. , & Sturmbauer, C. (2012). Population dynamics with a mixed type of sexual and asexual reproduction in a fluctuating environment. BMC Evolutionary Biology, 12, 49. PubMed PMC

Bateson, W. (1909). Heredity and variation in modern lights. In Darwin and modern science (pp. 85–101). Cambridge University Press.

Bengtsson, B. O. (2009). Asex and evolution: A very large‐scale overview. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex (pp. 1–19). Springer.

Berger, L. (1983). Western palearctic water frogs (Amphibia, Ranidae): Systematics, genetics and population compositions. Experientia, 39, 127–130.

Bernstein, H. , & Bernstein, C. (2010). Evolutionary origin of recombination during meiosis. Bioscience, 60, 498–505.

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

Bi, K. , Bogart, J. P. , & Fu, J. (2008). The prevalence of genome replacement in unisexual salamanders of the genus Ambystoma (Amphibia, Caudata) revealed by nuclear gene genealogy. BMC Evolutionary Biology, 8, 158. PubMed PMC

Binet, M.‐C. , & Angers, B. (2005). Genetic identification of members of the Phoxinus eos‐neogaeus hybrid complex. Journal of Fish Biology, 67, 1169–1177.

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). Springer.

Bogart, J. P. (2019). Unisexual salamanders in the genus Ambystoma . Herpetologica, 75, 259–267.

Bogart, J. P. , Bartoszek, J. , Noble, D. W. A. , & Bi, K. (2009). Sex in unisexual salamanders: Discovery of a new sperm donor with ancient affinities. Heredity, 103, 483–493. PubMed

Bolnick, D. I. , & Near, T. J. (2005). Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution, 59, 1754–1767. PubMed

Boyer, L. , Jabbour‐Zahab, R. , Joncour, P. , Glémin, S. , Haag, C. R. , & Lenormand, T. (2023). Asexual male production by ZW recombination in Artemia parthenogenetica . Evolution, 77, 1–12. PubMed

Brockhurst, M. A. , Chapman, T. , King, K. C. , Mank, J. E. , Paterson, S. , & Hurst, G. D. D. (2014). Running with the Red Queen: The role of biotic conflicts in evolution. Proceedings of the Royal Society B: Biological Sciences, 281, 20141382. PubMed PMC

Butlin, R. K. , Schön, I. , & Martens, K. (1999). Origin, age and diversity of clones. Journal of Evolutionary Biology, 12, 1020–1022.

Byers, D. L. , & Waller, D. M. (1999). Do plant populations purge their genetic load? Effects of population size and mating history on inbreeding depression. Annual Review of Ecology and Systematics, 30, 479–513.

Carman, J. G. (1997). Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biological Journal of the Linnean Society, 61, 51–94.

Carman, J. G. , Mateo de Arias, M. , Gao, L. , Zhao, X. , Kowallis, B. M. , Sherwood, D. A. , Srivastava, M. K. , Dwivedi, K. K. , Price, B. J. , Watts, L. , & Windham, M. D. (2019). Apospory and Diplospory in diploid Boechera (Brassicaceae) may facilitate speciation by recombination‐driven Apomixis‐to‐sex reversals. Frontiers in Plant Science, 10, 724. PubMed PMC

Charlesworth, B. , & Charlesworth, D. (1978). A model for the evolution of dioecy and gynodioecy. The American Naturalist, 112, 975–997.

Choleva, L. , Apostolou, A. , Ráb, P. , & Janko, K. (2008). Making it on their own: Sperm‐dependent hybrid fishes (Cobitis) switch the sexual hosts and expand beyond the ranges of their original sperm donors. Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2911–2919. PubMed PMC

Choleva, L. , & Janko, K. (2013). Rise and persistence of animal polyploidy: Evolutionary constraints and potential. Cytogenetic and Genome Research, 140, 151–170. PubMed

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, 2191–2203. PubMed

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, e80641. PubMed PMC

Christiansen, D. G. , Fog, K. , Pedersen, B. V. , & Boomsma, J. J. (2005). Reproduction and hybrid load in all‐hybrid populations of Rana esculenta water frogs in Denmark. Evolution, 59, 1348–1361. PubMed

Christiansen, D. G. , & Reyer, H.‐U. (2009). From clonal to sexual hybrids: Genetic recombination via triploids in all‐hybrid populations of water frogs. Evolution, 63, 1754–1768. PubMed

Cohan, F. M. (2001). Bacterial species and speciation. Systematic Biology, 50, 513–524. PubMed

Cohan, F. M. (2002). Sexual isolation and speciation in bacteria. Genetica, 116, 359–370. PubMed

Cosentino, B. J. , Phillips, C. A. , Schooley, R. L. , Lowe, W. H. , & Douglas, M. R. (2012). Linking extinction–colonization dynamics to genetic structure in a salamander metapopulation. Proceedings of the Biological Sciences, 279, 1575–1582. PubMed PMC

Coyne, J. A. , & Orr, H. A. (2004). Speciation (Illustrated ed.). Sinauer Associates.

Cunha, C. , Doadrio, I. , & Coelho, M. M. (2008). Speciation towards tetraploidization after intermediate processes of non‐sexual reproduction. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363, 2921–2929. PubMed PMC

Dalziel, A. C. , Tirbhowan, S. , Drapeau, H. F. , Power, C. , Jonah, L. S. , Gbotsyo, Y. A. , & Dion‐Côté, A.‐M. (2020). Using asexual vertebrates to study genome evolution and animal physiology: Banded (Fundulus diaphanus) × common killifish (F. heteroclitus) hybrid lineages as a model system. Evolutionary Applications, 13, 1214–1239. PubMed PMC

Darlington, C. D. (1939). The evolution of genetic systems. Annals of the Entomological Society of America, 32, 656–657.

De Storme, N. , & Mason, A. (2014). Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Current Plant Biology, 1, 10–33.

Debortoli, N. , Li, X. , Eyres, I. , Fontaneto, D. , Hespeels, B. , Tang, C. Q. , Flot, J.‐F. , & Van Doninck, K. (2016). Genetic exchange among bdelloid rotifers is more likely due to horizontal gene transfer than to meiotic sex. Current Biology, 26, 723–732. PubMed

Dedukh, D. , Majtánová, Z. , Marta, A. , Pšenička, M. , Kotusz, J. , Klíma, J. , 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, 215, 975–987. PubMed PMC

Dedukh, D. , Marta, A. , & Janko, K. (2021). Challenges and costs of asexuality: Variation in premeiotic genome duplication in gynogenetic hybrids from Cobitis taenia complex. International Journal of Molecular Sciences, 22, 12117. PubMed PMC

Denton, R. D. , Morales, A. E. , & Gibbs, H. L. (2018). Genome‐specific histories of divergence and introgression between an allopolyploid unisexual salamander lineage and two ancestral sexual species. Evolution, 72, 1689–1700. PubMed

Domes, K. , Norton, R. A. , Maraun, M. , & Scheu, S. (2007). Reevolution of sexuality breaks Dollo's law. Proceedings of the National Academy of Sciences of the United States of America, 104, 7139–7144. PubMed PMC

D'Souza, T. G. , & Michiels, N. K. (2009). Sex in parthenogenetic planarians: Phylogenetic relic or evolutionary resurrection? In Schön I., Martens K., & Dijk P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis (pp. 377–397). Springer.

D'Souza, T. G. , & Michiels, N. K. (2010). The costs and benefits of occasional sex: Theoretical predictions and a case study. Journal of Heredity, 101, S34–S41. PubMed

Dubey, S. , Maddalena, T. , Bonny, L. , Jeffries, D. L. , & Dufresnes, C. (2019). Population genomics of an exceptional hybridogenetic system of Pelophylax water frogs. BMC Evolutionary Biology, 19, 164. PubMed PMC

Dubois, A. (2011). Species and “strange species” in zoology: Do we need a “unified concept of species”? Comptes Rendus Palevol, 10, 77–94.

Edmands, S. (2002). Does parental divergence predict reproductive compatibility? Trends in Ecology & Evolution, 17, 520–527.

Ernst, A. (1918). Bastardierung als Ursache der Apogamie im Pflanzenreich. Eine Hypothese zur experimentellen Vererbungs‐ und Abstammungslehre. Nabu Press.

Fehrer, J. , Šimek, R. , Krahulcová, A. , Krahulec, F. , Chrtek, J. , Brautigam, E. , & Bräutigam, S. (2005). Evolution, hybridization, and clonal distribution of apo‐ and amphimictic species of Hieracium subgen. Pilosella Asteraceae, Lactucaceae in a Central European mountain range. In Bakker F., Chatrou L., Gravendeel B., & Pelser P. B. (Eds.), Plant species‐level systematics: New perspectives on pattern and process (pp. 175–201). Gantner Verlag.

Fontaneto, D. , Herniou, E. A. , Boschetti, C. , Caprioli, M. , Melone, G. , Ricci, C. , & Barraclough, T. G. (2007). Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5, e87. PubMed PMC

Forsgren, E. , Amundsen, T. , Borg, Å. A. , & Bjelvenmark, J. (2004). Unusually dynamic sex roles in a fish. Nature, 429, 551–554. PubMed

Franklin, L. R. (2007). Bacteria, sex, and systematics. Philosophy of Science, 74, 69–95.

Fujita, M. K. , Singhal, S. , Brunes, T. O. , & Maldonado, J. A. (2020). Evolutionary dynamics and consequences of parthenogenesis in vertebrates. Annual Review of Ecology, Evolution, and Systematics, 51, 191–214.

Fyon, F. , Berbel‐Filho, W. M. , Schlupp, I. , Wild, G. , & Úbeda, F. (2023). Why do hybrids turn down sex? Evolution, qpad129. In press. PubMed

Gabor, C. R. , da Barbiano, L. A. , & Aspbury, A. S. (2013). Geographic variation in male mate choice in a gynogenetic species complex: Evaluating long‐term data across mating contexts. Evolutionary Ecology Research, 15, 653–666.

Gabor, C. R. , & Ryan, M. J. (2001). Geographical variation in reproductive character displacement in mate choice by male sailfin mollies. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268, 1063–1070. PubMed PMC

Gabor, C. R. , Ryan, M. J. , & Morizot, D. C. (2005). Character displacement in sailfin mollies, Poecilia latipinna: Allozymes and behavior. Environmental Biology of Fishes, 73, 75–88.

Glémin, S. , François, C. M. , & Galtier, N. (2019). Genome evolution in outcrossing vs. selfing vs. asexual species. In Anisimova M. (Ed.), Evolutionary genomics: Statistical and computational methods (pp. 331–369). Springer. PubMed

Goddard, K. A. , & Schultz, R. J. (1993). Aclonal reproduction by polyploid members of the clonal hybrid species Phoxinus eos‐neogaeus (Cyprinidae). Copeia, 1993, 650–660.

Graf, J.‐D. , & Polls‐Pelaz, M. (1989). Evolutionary genetics of the Rana esculenta complex. In Dawley R. M. & Bogart J. P. (Eds.), Evolution and ecology of unisexual vertebrates. Bulletin 466 (pp. 289–301). New York State Museum.

Grosmaire, M. , Launay, C. , Siegwald, M. , Brugière, T. , Estrada‐Virrueta, L. , Berger, D. , Burny, C. , Modolo, L. , Blaxter, M. , Meister, P. , Félix, M.‐A. , Gouyon, P.‐H. , & Delattre, M. (2019). Males as somatic investment in a parthenogenetic nematode. Science, 363, 1210–1213. PubMed

Hausdorf, B. (2011). Progress toward a general species concept. Evolution, 65, 923–931. PubMed

Hedtke, S. M. , & Hillis, D. M. (2011). The potential role of androgenesis in cytoplasmic‐nuclear phylogenetic discordance. Systematic Biology, 60, 87–96. PubMed

Hedtke, S. M. , Stanger‐Hall, K. , Baker, R. J. , & Hillis, D. M. (2008). All‐male asexuality: Origin and maintenance of androgenesis in the Asian clam corbicula. Evolution, 62, 1119–1136. PubMed

Hernández Chávez, C. , & Turgeon, J. (2007). Asexual and sexual hybrids between Fundulus diaphanus and F. heteroclitus in the Canadian Atlantic region. Molecular Ecology, 16, 1467–1480. PubMed

Heubel, K. U. , & Schlupp, I. (2008). Seasonal plasticity in male mating preferences in sailfin mollies. Behavioral Ecology, 19, 1080–1086.

Hoffmann, A. , Plötner, J. , Pruvost, N. B. M. , Christiansen, D. G. , Röthlisberger, S. , Choleva, L. , Mikulíček, P. , Cogălniceanu, D. , Sas‐Kovács, I. , Shabanov, D. , Morozov‐Leonov, S. , & Reyer, H.‐U. (2015). Genetic diversity and distribution patterns of diploid and polyploid hybrid water frog populations (Pelophylax esculentus complex) across Europe. Molecular Ecology, 24, 4371–4391. PubMed

Hojsgaard, D. , & Hörandl, E. (2015). Apomixis as a facilitator of range expansion and diversification in plants. In Pontarotti P. (Ed.), Evolutionary biology: Biodiversification from genotype to phenotype (pp. 305–327). Springer International Publishing.

Holt, R. D. , & Bonsall, M. B. (2017). Apparent competition. Annual Review of Ecology, Evolution, and Systematics, 48, 447–471.

Hörandl, E. , & Hojsgaard, D. (2012). The evolution of apomixis in angiosperms: A reappraisal. Plant Biosystems – An International Journal Dealing with all Aspects of Plant Biology, 146, 681–693.

Hörandl, E. , & Paun, O. (2007). Patterns and sources of genetic diversity in apomictic plants: Implications for evolutionary potentials. In Hörandl E., Grossniklaus U., Sharbel T., & van Dijk P. (Eds.), Apomixis: Evolution, mechanisms, and perspectives (pp. 169–194). A.R.G. Gantner Verlag.

Hotz, H. , Beerli, P. , & Spolsky, C. (1992). Mitochondrial DNA reveals formation of nonhybrid frogs by natural matings between hemiclonal hybrids. Molecular Biology and Evolution, 9, 610–620. PubMed

Hotz, H. , Mancino, G. , Bucciinnocenti, S. , Ragghianti, M. , Berger, L. , & Uzzell, T. (1985). Rana ridibunda varies geographically in inducing clonal gametogenesis in interspecies hybrids. Journal of Experimental Zoology, 236, 199–210.

Hubbs, C. (1964). Interactions between a bisexual fish species and its gynogenetic sexual parasite. The Bulletin of the Texas Memorial Museum, 8, 1–72.

Hubbs, C. L. , & Hubbs, L. C. (1932). Apparent parthenogenesis in nature, in a form of fish of hybrid origin. Science, 76, 628–630. PubMed

Husband, B. C. (2000). Constraints on polyploid evolution: A test of the minority cytotype exclusion principle. Proceedings of the Biological Sciences, 267, 217–223. PubMed PMC

Jablonska, O. , Juchno, D. , Leska, A. , Kowalewska, K. , & Boroń, A. (2020). The variable occurrence of apoptosis in the testes of diploid and sterile allotetraploid Cobitis (Teleostei, Cobitidae) males during the reproductive cycle. Journal of Experimental Biology, 223, jeb212050. 10.1242/jeb.212050 PubMed DOI

Jalinsky, J. , Logsdon, J. M. , & Neiman, M. (2020). Male phenotypes in a female framework: Evidence for degeneration in sperm produced by male snails from asexual lineages. Journal of Evolutionary Biology, 33, 1050–1059. PubMed

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, 2991–3004. PubMed

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. PubMed PMC

Janko, K. , & Eisner, J. (2009). Sperm‐dependent parthenogens delay the spatial expansion of their sexual hosts. Journal of Theoretical Biology, 261, 431–440. PubMed

Janko, K. , Eisner, J. , & Mikulíček, P. (2019). Sperm‐dependent asexual hybrids determine competition among sexual species. Scientific Reports, 9, 722. PubMed PMC

Janko, K. , Flajšhans, M. , Choleva, L. , Bohlen, J. , Šlechtová, V. , Rábová, M. , Lajbner, Z. , Šlechta, V. , Ivanova, P. , Dobrovolov, I. , Culling, M. , Persat, H. , Kotusz, J. , & 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.

Janko, K. , Kotusz, J. , De Gelas, K. , Slechtová, V. , Opoldusová, Z. , Drozd, P. , Choleva, L. , Popiołek, M. , & 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, e45384. PubMed PMC

Janko, K. , Pačes, J. , Wilkinson‐Herbots, H. , Costa, R. J. , Roslein, J. , Drozd, P. , Iakovenko, N. , Rídl, J. , Hroudová, M. , Kočí, J. , Reifová, R. , Šlechtová, V. , & 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. PubMed PMC

Juchno, D. , & Boroń, A. (2006). Comparative histology of the testes of the spined loach Cobitis taenia L. and natural allotetraploids of Cobitis (Pisces, Cobitidae). Hydrobiologia, 573, 45–53.

Kočí, J. , Röslein, J. , Pačes, J. , Kotusz, J. , Halačka, K. , Koščo, J. , Fedorčák, J. , Iakovenko, N. , & Janko, K. (2020). No evidence for accumulation of deleterious mutations and fitness degradation in clonal fish hybrids: Abandoning sex without regrets. Molecular Ecology, 29, 3038–3055. PubMed PMC

Kokko, H. , Heubel, K. U. , & Rankin, D. J. (2008). How populations persist when asexuality requires sex: The spatial dynamics of coping with sperm parasites. Proceedings of the Biological Sciences, 275, 817–825. PubMed PMC

Koonin, E. V. , Makarova, K. S. , & Aravind, L. (2001). Horizontal gene transfer in prokaryotes: Quantification and classification. Annual Review of Microbiology, 55, 709–742. PubMed PMC

Kuroda, M. , Fujimoto, T. , Murakami, M. , Yamaha, E. , & Arai, K. (2018). Clonal reproduction assured by sister chromosome pairing in dojo loach, a teleost fish. Chromosome Research, 26, 243–253. PubMed

Kwan, Y.‐S. , Ko, M.‐H. , Jeon, Y.‐S. , Kim, H.‐J. , & Won, Y.‐J. (2019). Bidirectional mitochondrial introgression between Korean cobitid fish mediated by hybridogenetic hybrids. Ecology and Evolution, 9, 1244–1254. PubMed PMC

Lacy, R. C. (1987). Loss of genetic diversity from managed populations: Interacting effects of drift, mutation, immigration, selection, and population subdivision. Conservation Biology, 1, 143–158.

Lampert, K. P. , Lamatsch, D. K. , Fischer, P. , Epplen, J. T. , Nanda, I. , Schmid, M. , & Schartl, M. (2007). Automictic reproduction in interspecific hybrids of poeciliid fish. Current Biology, 17, 1948–1953. PubMed

Lampert, K. P. , & Schartl, M. (2008). The origin and evolution of a unisexual hybrid: Poecilia formosa . Philosophical Transactions of the Royal Society B: Biological Sciences, 363, 2901–2909. PubMed PMC

Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution, 30, 314–334. PubMed

Laskowski, K. L. , Doran, C. , Bierbach, D. , Krause, J. , & Wolf, M. (2019). Naturally clonal vertebrates are an untapped resource in ecology and evolution research. Nature Ecology & Evolution, 3, 161–169. PubMed

Lehtonen, J. , Schmidt, D. J. , Heubel, K. , & Kokko, H. (2013). Evolutionary and ecological implications of sexual parasitism. Trends in Ecology & Evolution, 28, 297–306. PubMed

Lievens, E. J. P. , Henriques, G. J. B. , Michalakis, Y. , & Lenormand, T. (2016). Maladaptive sex ratio adjustment in the invasive brine shrimp Artemia franciscana . Current Biology, 26, 1463–1467. PubMed

Lively, C. M. , & Morran, L. T. (2014). The ecology of sexual reproduction. Journal of Evolutionary Biology, 27, 1292–1303. PubMed PMC

Lowe, W. H. , & Allendorf, F. W. (2010). What can genetics tell us about population connectivity? Molecular Ecology, 19, 3038–3051. PubMed

Majeský, Ľ. , Vašut, R. J. , Kitner, M. , & Trávníček, B. (2012). The pattern of genetic variability in apomictic clones of Taraxacum officinale indicates the alternation of asexual and sexual histories of apomicts. PLoS One, 7, e41868. PubMed PMC

Makowicz, A. M. , & Schlupp, I. (2015). Effects of female‐female aggression in a sexual/unisexual species complex. Ethology, 121, 903–914.

Marshall, J. L. , Arnold, M. L. , & Howard, D. J. (2002). Reinforcement: The road not taken. Trends in Ecology & Evolution, 17, 558–563.

Marta, A. , Tichopád, T. , Bartoš, O. , Klíma, J. , Shah, M. A. , Bohlen, V. Š. , Bohlen, J. , Halačka, K. , Choleva, L. , Stöck, M. , Dedukh, D. , & Janko, K. (2023). Genetic and karyotype divergence between parents affect clonality and sterility in hybrids. eLife, 2, RP88366. 10.7554/eLife.88366.1. In press. PubMed DOI PMC

Matute, D. R. , Butler, I. A. , Turissini, D. A. , & Coyne, J. A. (2010). A test of the snowball theory for the rate of evolution of hybrid incompatibilities. Science, 329, 1518–1521. PubMed

Mee, J. A. , & Otto, S. P. (2010). Variation in the strength of male mate choice allows long‐term coexistence of sperm‐dependent asexuals and their sexual hosts. Evolution, 64, 2808–2819. PubMed

Meirmans, S. (2009). The evolution of the problem of sex. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis (pp. 21–46). Springer.

Mikulíček, P. , Kautman, M. , Demovič, B. , & Janko, K. (2014). When a clonal genome finds its way back to a sexual species: Evidence from ongoing but rare introgression in the hybridogenetic water frog complex. Journal of Evolutionary Biology, 27, 628–642. PubMed

Mikulíček, P. , Kautman, M. , Kautman, J. , & Pruvost, N. B. M. (2015). Mode of hybridogenesis and habitat preferences influence population composition of water frogs (Pelophylax esculentus complex, Anura: Ranidae) in a region of sympatric occurrence (western Slovakia). Journal of Zoological Systematics and Evolutionary Research, 53, 124–132.

Mirzaghaderi, G. , & Hörandl, E. (2016). The evolution of meiotic sex and its alternatives. Proceedings of the Biological Sciences, 283, 20161221. PubMed PMC

Morgado‐Santos, M. , Pereira, H. M. , Vicente, L. , & Collares‐Pereira, M. J. (2015). Mate choice drives evolutionary stability in a hybrid complex. PLoS One, 10, e0132760. PubMed PMC

Moritz, C. , Brown, W. M. , Densmore, L. D. , Wright, J. W. , Vyas, D. , Donnellan, S. , Adams, M. , & Baverstock, P. (1989). Genetic diversity and the dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae). In Dawley R. M. & Bogart J. P. (Eds.), Evolution and ecology of unisexual vertebrates. Bulletin 466 (pp. 268–280). New York State Museum.

Neaves, W. B. , & Baumann, P. (2011). Unisexual reproduction among vertebrates. Trends in Genetics, 27, 81–88. PubMed

Neiman, M. , & Linksvayer, T. A. (2006). The conversion of variance and the evolutionary potential of restricted recombination. Heredity, 96, 111–121. PubMed

Neiman, M. , Sharbel, T. F. , & Schwander, T. (2014). Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. Journal of Evolutionary Biology, 27, 1346–1359. PubMed

Ortiz‐Barrientos, D. , Engelstädter, J. , & Rieseberg, L. H. (2016). Recombination rate evolution and the origin of species. Trends in Ecology & Evolution, 31, 226–236. PubMed

Pagano, A. , Lodé, T. , & Crochet, P.‐A. (2001). New contact zone and assemblages among water frogs of southern France. Journal of Zoological Systematics and Evolutionary Research, 39, 63–67.

Paland, S. , Colbourne, J. K. , & Lynch, M. (2005). Evolutionary history of contagious asexuality in Daphnia pulex . Evolution, 59, 800–813. PubMed

Pantel, J. H. , Juenger, T. E. , & Leibold, M. A. (2011). Environmental gradients structure Daphnia pulex × pulicaria clonal distribution. Journal of Evolutionary Biology, 24, 723–732. PubMed

Parker, D. J. , Bast, J. , Jalvingh, K. , Dumas, Z. , Robinson‐Rechavi, M. , & Schwander, T. (2019). Repeated evolution of asexuality involves convergent gene expression changes. Molecular Biology and Evolution, 36, 350–364. PubMed PMC

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, 5908–5921. PubMed

Pigneur, L.‐M. , Hedtke, S. M. , Etoundi, E. , & Van Doninck, K. (2012). Androgenesis: A review through the study of the selfish shellfish corbicula spp. Heredity (Edinb), 108, 581–591. PubMed PMC

Pigneur, L.‐M. , Marescaux, J. , Roland, K. , Etoundi, E. , Descy, J.‐P. , & Van Doninck, K. (2011). Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe. BMC Evolutionary Biology, 11, 147. PubMed PMC

Plötner, J. , Uzzell, T. , Beerli, P. , Spolsky, C. , Ohst, T. , Litvinchuk, S. N. , Guex, G.‐D. , Reyer, H.‐U. , & Hotz, H. (2008). Widespread unidirectional transfer of mitochondrial DNA: A case in western Palaearctic water frogs. Journal of Evolutionary Biology, 21, 668–681. PubMed PMC

Pruvost, N. B. M. , Mikulíček, P. , Choleva, L. , & Reyer, H.‐U. (2015). Contrasting reproductive strategies of triploid hybrid males in vertebrate mating systems. Journal of Evolutionary Biology, 28, 189–204. PubMed

Redfield, R. J. (1994). Male mutation rates and the cost of sex for females. Nature, 369, 145–147. PubMed

Rieseberg, L. H. , & Willis, J. H. (2007). Plant speciation. Science, 317, 910–914. PubMed PMC

Ross, L. , Hardy, N. B. , Okusu, A. , & Normark, B. B. (2012). Large population size predicts the distribution of asexuality in scale insects. Evolution, 67, 196–206. PubMed

Russell, S. (2003). Evolution of intrinsic post‐zygotic reproductive isolation in fish. Annales Zoologici Fennici, 40, 321–329.

Sailer, C. , Stöcklin, J. , & Grossniklaus, U. (2020). Dynamics of apomictic and sexual reproduction during primary succession on a glacier forefield in the Swiss Alps. Scientific Reports, 10, 8269. PubMed PMC

Sankararaman, S. , Mallick, S. , Dannemann, M. , Prüfer, K. , Kelso, J. , Pääbo, S. , Patterson, N. , & Reich, D. (2014). The landscape of neandertal ancestry in present‐day humans. Nature, 507, 354–357. PubMed PMC

Scali, V. (2009). Metasexual stick insects: Model pathways to losing sex and bringing it back. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis (pp. 317–345). Springer.

Schartl, M. , Nanda, I. , Schlupp, I. , Wilde, B. , Epplen, J. T. , Schmid, M. , & Parzefall, J. (1995). Incorporation of subgenomic amounts of DNA as compensation for mutational load in a gynogenetic fish. Nature, 373, 68–71.

Schartl, M. , Schlupp, I. , Schartl, A. , Meyer, M. K. , Nanda, I. , Schmid, M. , Epplen, J. T. , & Parzefall, J. (1991). On the stability of dispensable constituents of the eukaryotic genome: Stability of coding sequences versus truly hypervariable sequences in a clonal vertebrate, the amazon molly, Poecilia formosa . PNAS, 88, 8759–8763. PubMed PMC

Schlupp, I. (2005). The evolutionary ecology of gynogenesis. Annual Review of Ecology, Evolution, and Systematics, 36, 399–417.

Schlupp, I. (2009). Chapter 5 behavior of fishes in the sexual/unisexual mating system of the Amazon molly (Poecilia formosa). In Advances in the study of behavior (pp. 153–183). Academic Press.

Schlupp, I. (2010). Mate choice and the Amazon molly: How sexuality and unisexuality can coexist. Journal of Heredity, 101, S55–S61. PubMed

Schlupp, I. (2021). Male choice, female competition, and female ornamentation in sexual selection. Oxford University Press.

Schlupp, I. , Nanda, I. , Döbler, M. , Lamatsch, D. K. , Epplen, J. T. , Parzefall, J. , Schmid, M. , & Schartl, M. (1998). Dispensable and indispensable genes in an ameiotic fish, the Amazon molly Poecilia formosa . Cytogenetics and Cell Genetics, 80, 193–198. PubMed

Schlupp, I. , Parzefall, J. , Epplen, J. T. , Nanda, I. , Schmid, M. , & Schartl, M. (1992). Pseudomale behaviour and spontaneous masculinization in the all‐female teleost Poecilia formosa (Teleostei: Poeciliidae). Behaviour, 122, 88–104.

Schlupp, I. , Parzefall, J. , & Schartl, M. (2002). Biogeography of the Amazon molly, Poecilia formosa . Journal of Biogeography, 29, 1–6.

Schlupp, I. , & Plath, M. (2005). Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei). Biology Letters, 1, 169–171. PubMed PMC

Schlupp, I. , & Riesch, R. (2011). Evolution of unisexual reproduction. In Evans J., Pilastro A. & Schlupp I. (Eds.), Ecology and evolution of poeciliid fishes (pp. 50–58). University of Chicago.

Schmeller, D. S. , Seitz, A. , Crivelli, A. , & Veith, M. (2005). Crossing species' range borders: Interspecies gene exchange mediated by hybridogenesis. Proceedings of the Biological Sciences, 272, 1625–1631. PubMed PMC

Schön, I. , Pinto, R. L. , Halse, S. , Smith, A. J. , Martens, K. , & Birky, C. W. (2012). Cryptic species in putative ancient asexual darwinulids (Crustacea, Ostracoda). PLoS One, 7, e39844. PubMed PMC

Schultz, R. J. (1973). Unisexual fish: Laboratory synthesis of a “species”. Science, 179, 180–181. PubMed

Seehausen, O. , Butlin, R. K. , Keller, I. , Wagner, C. E. , Boughman, J. W. , Hohenlohe, P. A. , Peichel, C. L. , Saetre, G.‐P. , Bank, C. , Brännström, Å. , Brelsford, A. , Clarkson, C. S. , Eroukhmanoff, F. , Feder, J. L. , Fischer, M. C. , Foote, A. D. , Franchini, P. , Jiggins, C. D. , Jones, F. C. , … Widmer, A. (2014). Genomics and the origin of species. Nature Reviews Genetics, 15, 176–192. PubMed

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. PubMed PMC

Signorovitch, A. , Hur, J. , Gladyshev, E. , & Meselson, M. (2015). Allele sharing and evidence for sexuality in a mitochondrial clade of Bdelloid rotifers . Genetics, 200, 581–590. PubMed PMC

Simion, P. , Narayan, J. , Houtain, A. , Derzelle, A. , Baudry, L. , Nicolas, E. , Arora, R. , Cariou, M. , Cruaud, C. , Gaudray, F. R. , Gilbert, C. , Guiglielmoni, N. , Hespeels, B. , Kozlowski, D. K. L. , Labadie, K. , Limasset, A. , Llirós, M. , Marbouty, M. , Terwagne, M. , … Van Doninck, K. (2021). Chromosome‐level genome assembly reveals homologous chromosomes and recombination in asexual rotifer Adineta vaga . Science Advances, 7, eabg4216. PubMed PMC

Skierska, K. , Lagner, A. , Rozenblut‐Kościsty, B. , Kosiba, P. , Kolenda, K. , & Ogielska, M. (2023). Population structure, mate choice, and genome transmission in naturally formed pairs in a Pelophylax lessonae–Pelophylax esculentus hybridogenetic system. Behavioral Ecology and Sociobiology, 77, 92.

Slyn'ko, Y. V. (2000). Sistema razmnozheniya mezhrodovykh gibridov plotvy (Rutilus rutilus L.), leshcha (Abramis brama L.) i sinca (Abramis ballerus L.) (Leuciscinae: Cyprinidae) (PhD thesis). http://www.dissercat.com/content/sistema‐razmnozheniya‐mezhrodovykh‐gibridov‐plotvy‐rutilus‐rutilus‐l‐leshcha‐abramis‐brama‐l

Sochor, M. , Šarhanová, P. , Pfanzelt, S. , & Trávníček, B. (2017). Is evolution of apomicts driven by the phylogeography of the sexual ancestor? Insights from European and Caucasian brambles (Rubus, Rosaceae). Journal of Biogeography, 44, 2717–2728.

Sousa‐Santos, C. , Collares‐Pereira, M. J. , & Almada, V. C. (2006). Evidence of extensive mitochondrial introgression with nearly complete substitution of the typical Squalius pyrenaicus‐like mtDNA of the Squalius alburnoides complex (Cyprinidae) in an independent Iberian drainage. Journal of Fish Biology, 68, 292–301.

Stenberg, P. , & Saura, A. (2009). Cytology of asexual animals. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex (pp. 63–74). Springer.

Stenberg, P. , & Saura, A. (2013). Meiosis and its deviations in polyploid animals. Cytogenetic and Genome Research, 140, 185–203. PubMed

Stöck, M. , Dedukh, D. , Reifová, R. , Lamatsch, D. K. , Starostová, Z. , & Janko, K. (2021). Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: Along the ‘extended speciation continuum’. Philosophical Transactions of the Royal Society B: Biological Sciences, 376, 20200103. PubMed PMC

Stöck, M. , Lamatsch, D. K. , Steinlein, C. , Epplen, J. T. , Grosse, W.‐R. , Hock, R. , Klapperstück, T. , Lampert, K. P. , Scheer, U. , Schmid, M. , & Schartl, M. (2002). A bisexually reproducing all‐triploid vertebrate. Nature Genetics, 30, 325–328. PubMed

Stöck, M. , Lampert, K. P. , Möller, D. , Schlupp, I. , & Schartl, M. (2010). Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa). Molecular Ecology, 19, 5204–5215. PubMed

Stork, S. , Jalinski, J. , & Neiman, M. (2022). Evidence for stronger discrimination between conspecific and heterospecific mating partners in sexual vs. asexual female freshwater snails. PeerJ, 10, e14470. PubMed PMC

Suzuki, S. , Miyake, S. , Arai, K. , & Munehara, H. (2019). Unisexual hybrids break through an evolutionary dead end by two‐way backcrossing. Evolution, 74, 392–403. 10.1111/evo.13903 PubMed DOI

Thomas, F. , Guégan, J. , Michalakis, Y. , & Renaud, F. (2000). Parasites and host life‐history traits: Implications for community ecology and species co‐existence. International Journal for Parasitology, 30, 669–674. PubMed

Thompson, M. J. , & Jiggins, C. D. (2014). Supergenes and their role in evolution. Heredity (Edinb), 113, 1–8. PubMed PMC

Uzzell, T. , & Berger, L. (1975). Electrophoretic phenotypes of Rana ridibunda, Rana lessonae, and their hybridogenetic associate, Rana esculenta . Proceedings of the Academy of Natural Sciences of Philadelphia, 127, 13–24.

Uzzell, T. , Günther, R. , & Berger, L. (1977). Rana ridibunda and Rana esculenta: A leaky hybridogenetic system (Amphibia Salientia). Proceedings of the Academy of Natural Sciences of Philadelphia, 128, 147–171.

Van der Kooi, C. J. , Matthey‐Doret, C. , & Schwander, T. (2017). Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evolution Letters, 1, 304–316. PubMed PMC

van der Kooi, C. J. , & Schwander, T. (2014). On the fate of sexual traits under asexuality. Biological Reviews of the Cambridge Philosophical Society, 89, 805–819. PubMed

Van Dijk, P. (2009). Apomixis: Basics for non‐botanists. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex (pp. 47–62). Springer.

Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory, 1973, 1–30.

Vorburger, C. (2001). Non‐hybrid offspring from matings between hemiclonal hybrid waterfrogs suggest occasional recombination between clonal genomes. Ecology Letters, 4, 628–636.

Vrijenhoek, R. C. (1994). Unisexual fish: Model systems for studying ecology and evolution. Annual Review of Ecology and Systematics, 25, 71–96.

Vrijenhoek, R. C. , & Parker, E. D. (2009). Geographical parthenogenesis: General purpose genotypes and frozen niche variation. In Schön I., Martens K., & Dijk P. (Eds.), Lost sex: The evolutionary biology of parthenogenesis (pp. 99–131). Springer.

Warren, W. C. , García‐Pérez, R. , Xu, S. , Lampert, K. P. , Chalopin, D. , Stöck, M. , Loewe, L. , Lu, Y. , Kuderna, L. , Minx, P. , Montague, M. J. , Tomlinson, C. , Hillier, L. W. , Murphy, D. N. , Wang, J. , Wang, Z. , Garcia, C. M. , Thomas, G. C. W. , Volff, J.‐N. , … Schartl, M. (2018). Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nature Ecology & Evolution, 2, 669–679. PubMed 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. PubMed

Yadav, V. , Sun, S. , & Heitman, J. (2023). On the evolution of variation in sexual reproduction through the prism of eukaryotic microbes. Proceedings of the National Academy of Sciences, 120, e2219120120. PubMed PMC