1932

Abstract

Parthenogenesis is asexual reproduction without any required participation from males and, as such, is a null model for sexual reproduction. In a comparative context, we can expand our understanding of the evolution and ecology of sex by investigating the consequences of parthenogenesis. In this review, we examine the theoretical predictions of and empirical results on the evolution of asexual reproduction in vertebrates, focusing on recent studies addressing the origins and geographic spread of parthenogenetic lineages and the genomic consequences of an asexual life history. With advances in computational methods and genome technologies, researchers are poised to make rapid and significant progress in studying the origin and evolution of parthenogenesis in vertebrates, thus providing an important perspective on understanding biodiversity patterns of both asexual and sexual populations.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-011720-114900
2020-11-02
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/51/1/annurev-ecolsys-011720-114900.html?itemId=/content/journals/10.1146/annurev-ecolsys-011720-114900&mimeType=html&fmt=ahah

Literature Cited

  1. Abdala CS, Baldo D, Juárez RA, Espinoza RE 2016. The first parthenogenetic pleurodont iguanian: a new all-female Liolaemus (Squamata: Liolaemidae) from Western Argentina. Copeia 104:2487–97
    [Google Scholar]
  2. Abramjan A, Frýdlová P, Jančúchová-Lásková J, Suchomelová P, Landová E et al. 2019. Comparing developmental stability in unisexual and bisexual rock lizards of the genus Darevskia. Evol. Dev 21:4175–87
    [Google Scholar]
  3. Adams KL, Cronn R, Percifield R, Wendel JF 2003a. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. PNAS 100:84649–54
    [Google Scholar]
  4. Adams M, Foster R, Hutchinson MN, Hutchinson RG, Donnellan SC 2003b. The Australian scincid lizard Menetia greyii: a new instance of widespread vertebrate parthenogenesis. Evolution 57:112619–27
    [Google Scholar]
  5. Agrawal AF. 2006. Evolution of sex: Why do organisms shuffle their genotypes?. Curr. Biol. 16:17R696–704
    [Google Scholar]
  6. Amarasinghe SL, Su S, Dong X, Zappia L, Ritchie ME, Gouil Q 2020. Opportunities and challenges in long-read sequencing data analysis. Genome Biol 21:130
    [Google Scholar]
  7. Arakelyan M, Harutyunyan T, Aghayan SA, Carretero MA 2019. Infection of parthenogenetic lizards by blood parasites does not support the “Red Queen hypothesis” but reveals the costs of sex. Zoology 136:125709
    [Google Scholar]
  8. Avise JC. 2008. Clonality: The Genetics, Ecology, and Evolution of Sexual Abstinence in Vertebrate Animals New York: Oxford Univ. Press
  9. Barley AJ, Nieto-Montes de Oca A, Reeder TW, Manríquez-Morán NL, Arenas Monroy JC et al. 2019. Complex patterns of hybridization and introgression across evolutionary timescales in Mexican whiptail lizards (Aspidoscelis). Mol. Phylogenet. Evol. 132:284–95
    [Google Scholar]
  10. Bashir T, Sailer C, Gerber F, Loganathan N, Bhoopalan H et al. 2014. Hybridization alters spontaneous mutation rates in a parent-of-origin-dependent fashion in Arabidopsis. . Plant Physiol 165:1424–37
    [Google Scholar]
  11. Bast J, Jaron KS, Schuseil D, Roze D, Schwander T 2019. Asexual reproduction reduces transposable element load in experimental yeast populations. eLife 8:e48548
    [Google Scholar]
  12. Bast J, Parker DJ, Dumas Z, Jalvingh KM, Tran Van P et al. 2018. Consequences of asexuality in natural populations: insights from stick insects. Mol. Biol. Evol. 35:71668–77
    [Google Scholar]
  13. Bast J, Schaefer I, Schwander T, Maraun M, Scheu S, Kraaijeveld K 2016. No accumulation of transposable elements in asexual arthropods. Mol. Biol. Evol. 33:3697–706
    [Google Scholar]
  14. Bay RA, Harrigan RJ, Underwood VL, Gibbs HL, Smith TB, Ruegg K 2018. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science 359:637183–86
    [Google Scholar]
  15. Becks L, Agrawal AF. 2012. The evolution of sex is favoured during adaptation to new environments. PLOS Biol 10:5e1001317
    [Google Scholar]
  16. Bell G. 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality London: Croom Helm
  17. Birky CW Jr 1996. Heterozygosity, heteromorphy, and phylogenetic trees in asexual eukaryotes. Genetics 144:1427–37
    [Google Scholar]
  18. Blanckaert A, Bank C. 2018. In search of the Goldilocks zone for hybrid speciation. PLOS Genet 14:9e1007613
    [Google Scholar]
  19. Bolger DT, Case TJ. 1994. Divergent ecology of sympatric clones of the asexual gecko. Lepidodactylus lugubris. Oecologia 100:4397–405
    [Google Scholar]
  20. Booth W, Schuett GW. 2016. The emerging phylogenetic pattern of parthenogenesis in snakes. Biol. J. Linn. Soc. Lond. 118:2172–86
    [Google Scholar]
  21. Booth W, Smith CF, Eskridge PH, Hoss SK, Mendelson JR, Schuett GW 2012. Facultative parthenogenesis discovered in wild vertebrates. Biol. Lett. 8:6983–85
    [Google Scholar]
  22. Boussau B, Brown JM, Fujita MK 2011. Nonadaptive evolution of mitochondrial genome size. Evolution 65:92706–11
    [Google Scholar]
  23. Brandt A, Schaefer I, Glanz J, Schwander T, Maraun M et al. 2017. Effective purifying selection in ancient asexual oribatid mites. Nat. Commun. 8:1873
    [Google Scholar]
  24. Brunes TO, Silva AJ, Marques-Souza S, Rodrigues MT, Pellegrino KCM 2019. Not always young: the first vertebrate ancient origin of true parthenogenesis found in an Amazon leaf litter lizard with evidence of mitochondrial haplotypes surfing on the wave of a range expansion. Mol. Phylogenet. Evol. 135:105–22
    [Google Scholar]
  25. Castonguay E, Angers B. 2012. The key role of epigenetics in the persistence of asexual lineages. Genet. Res. Int. 2012:534289
    [Google Scholar]
  26. Charlesworth B. 1990. Mutation-selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55:3199–221
    [Google Scholar]
  27. Chen J-M, Cooper DN, Chuzhanova N, Férec C, Patrinos GP 2007. Gene conversion: mechanisms, evolution and human disease. Nat. Rev. Genet. 8:10762–75
    [Google Scholar]
  28. Cole CJ, Taylor HL, Neaves WB, Baumann DP, Newton A et al. 2017. The second known tetraploid species of parthenogenetic tetrapod (Reptilia: Squamata: Teiidae): description, reproduction, comparisons with ancestral taxa, and origins of multiple clones. Bull. Mus. Comp. Zool. 161:8285–321
    [Google Scholar]
  29. Cosentino BJ, Schooley RL, Bestelmeyer BT, Campos H, Burkett LM 2019. Does habitat disturbance promote geographical parthenogenesis in whiptail lizards. Evol. Ecol. 33:6839–53
    [Google Scholar]
  30. Costa GC, Schlupp I. 2010. Biogeography of the Amazon molly: ecological niche and range limits of an asexual hybrid species. Glob. Ecol. Biogeogr. 19:442–51
    [Google Scholar]
  31. Coyne JA, Orr HA. 2004. Speciation Sunderland, MA: Sinauer Associates
  32. Cuellar O. 1971. Reproduction and the mechanism of meiotic restitution in the parthenogenetic lizard Cnemidophorus uniparens. J. Morphol 133:2139–65
    [Google Scholar]
  33. Cuellar O. 1979. On the ecology of coexistence in parthenogenetic and bisexual lizards of the genus Cnemidophorus. Am. Zool 19:3773–86
    [Google Scholar]
  34. Cullum AJ. 1997. Comparisons of physiological performance in sexual and asexual whiptail lizards (genus Cnemidophorus): implications for the role of heterozygosity. Am. Nat. 150:124–47
    [Google Scholar]
  35. Daly M. 1978. The cost of mating. Am. Nat. 112:986771–74
    [Google Scholar]
  36. Danielyan F, Arakelyan M, Stepanyan I 2008. Hybrids of Darevskia valentini, D. armeniaca and D. unisexualis from a sympatric population in Armenia. Amphibia-Reptilia 29:487–504
    [Google Scholar]
  37. Darwin C. 1862. On the two forms, or dimorphic condition, in the species of Primula, and on their remarkable sexual relations. J. Proc. Linn. Soc. Bot. 6:77–96
    [Google Scholar]
  38. Decaestecker E, De Meester L, Mergeay J 2009. Cyclical parthenogenesis in Daphnia: sexual versus asexual reproduction. See Schön et al. 2009 295–316
  39. Desai MM, Fisher DS, Murray AW 2007. The speed of evolution and maintenance of variation in asexual populations. Curr. Biol. 17:5385–94
    [Google Scholar]
  40. Flot J-F, Hespeels B, Li X, Noel B, Arkhipova I et al. 2013. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. . Nature 500:7463453–57
    [Google Scholar]
  41. Freitas S, Rocha S, Campos J, Ahmadzadeh F, Corti C et al. 2016. Parthenogenesis through the ice ages: a biogeographic analysis of Caucasian rock lizards (genus Darevskia). Mol. Phylogenet. Evol. 102:117–27
    [Google Scholar]
  42. Fujita MK, Boore JL, Moritz C 2007. Multiple origins and rapid evolution of duplicated mitochondrial genes in parthenogenetic geckos (Heteronotia binoei; Squamata, Gekkonidae). Mol. Biol. Evol. 24:122775–86
    [Google Scholar]
  43. Gao Z, Moorjani P, Sasani TA, Pedersen BS, Quinlan AR et al. 2019. Overlooked roles of DNA damage and maternal age in generating human germline mutations. PNAS 116:199491–500
    [Google Scholar]
  44. Greenwald KR, Denton RD, Gibbs HL 2016. Niche partitioning among sexual and unisexual Ambystoma salamanders. Ecosphere 7:11e01579
    [Google Scholar]
  45. Griffing AH, Sanger TJ, Daza JD, Nielsen SV, Pinto BJ et al. 2019. Embryonic development of a parthenogenetic vertebrate, the mourning gecko (Lepidodactylus lugubris). Dev. Dyn. 248:111070–90
    [Google Scholar]
  46. Grismer JL, Bauer AM, Grismer LL, Thirakhupt K, Aowphol A et al. 2014. Multiple origins of parthenogenesis, and a revised species phylogeny for the Southeast Asian butterfly lizards. Leiolepis. Biol. J. Linn. Soc. Lond. 113:41080–93
    [Google Scholar]
  47. Gutekunst J, Andriantsoa R, Falckenhayn C, Hanna K, Stein W et al. 2018. Clonal genome evolution and rapid invasive spread of the marbled crayfish. Nat. Ecol. Evol. 2:3567–73
    [Google Scholar]
  48. Haig D. 2002. Genomic Imprinting and Kinship New Brunswick, NJ: Rutgers Univ. Press
  49. Hanley KA, Bolger DT, Case TJ 1994. Comparative ecology of sexual and asexual gecko species (Lepidodactylus) in French Polynesia. Evol. Ecol. 8:4438–54
    [Google Scholar]
  50. Hanley KA, Fisher RN, Case TJ 1995. Lower mite infestations in an asexual gecko compared with its sexual ancestors. Evolution 49:3418–26
    [Google Scholar]
  51. Harrison PW, Wright AE, Zimmer F, Dean R, Montgomery SH et al. 2015. Sexual selection drives evolution and rapid turnover of male gene expression. PNAS 112:144393–98
    [Google Scholar]
  52. Hegarty MJ, Barker GL, Wilson ID, Abbott RJ, Edwards KJ, Hiscock SJ 2006. Transcriptome shock after interspecific hybridization in Senecio is ameliorated by genome duplication. Curr. Biol. 16:161652–59
    [Google Scholar]
  53. Henry L, Schwander T, Crespi BJ 2012. Deleterious mutation accumulation in asexual Timema stick insects. Mol. Biol. Evol. 29:1401–8
    [Google Scholar]
  54. Hill WG, Robertson A. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:3269–94
    [Google Scholar]
  55. Hillis DM, Moritz C, Porter CA, Baker RJ 1991. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science 251:4991308–10
    [Google Scholar]
  56. Hollister JD, Greiner S, Wang W, Wang J, Zhang Y et al. 2015. Recurrent loss of sex is associated with accumulation of deleterious mutations in Oenothera. Mol. Biol. Evol 32:4896–905
    [Google Scholar]
  57. Hurst LD. 2009. Fundamental concepts in genetics: genetics and the understanding of selection. Nat. Rev. Genet. 10:283–93
    [Google Scholar]
  58. Jeffery KJ, Bangham CR. 2000. Do infectious diseases drive MHC diversity. Microbes Infect 2:111335–41
    [Google Scholar]
  59. Kearney M. 2005. Hybridization, glaciation and geographical parthenogenesis. Trends Ecol. Evol. 20:9495–502
    [Google Scholar]
  60. Kearney M, Fujita MK, Ridenour J 2009. Lost sex in the reptiles: constraints and correlations. See Schön et al. 2009 447–74
  61. Kearney M, Moussalli A, Strasburg J, Lindenmayer D, Moritz C 2003. Geographic parthenogenesis in the Australian arid zone: I. A climatic analysis of the Heteronotia binoei complex (Gekkonidae). Evol. Ecol. Res. 5:7953–76
    [Google Scholar]
  62. Kearney M, Shine R. 2004. Developmental success, stability, and plasticity in closely related parthenogenetic and sexual lizards (Heteronotia, Gekkonidae). Evolution 58:71560–72
    [Google Scholar]
  63. Kidwell MG, Lisch DR. 2000. Transposable elements and host genome evolution. Trends Ecol. Evol. 15:395–99
    [Google Scholar]
  64. Kondrashov AS. 1988. Deleterious mutations and the evolution of sexual reproduction. Nature 336:6198435–40
    [Google Scholar]
  65. Kong A, Frigge ML, Masson G, Besenbacher S, Sulem P et al. 2012. Rate of de novo mutations and the importance of father's age to disease risk. Nature 488:7412471–75
    [Google Scholar]
  66. Kono T, Obata Y, Wu Q, Niwa K, Ono Y et al. 2004. Birth of parthenogenetic mice that can develop to adulthood. Nature 428:6985860–64
    [Google Scholar]
  67. Laskowski KL, Doran C, Bierbach D, Krause J, Wolf M 2019. Naturally clonal vertebrates are an untapped resource in ecology and evolution research. Nat. Ecol. Evol. 3:2161–69
    [Google Scholar]
  68. Li C-Y, Li J-T, Kuang Y-Y, Xu R, Zhao Z-X et al. 2014. The transcriptomes of the crucian carp complex (Carassius auratus) provide insights into the distinction between unisexual triploids and sexual diploids. Int. J. Mol. Sci. 15:69386–406
    [Google Scholar]
  69. Lippman ZB, Zamir D. 2007. Heterosis: revisiting the magic. Trends Genet 23:260–66
    [Google Scholar]
  70. Lovell JT, Williamson RJ, Wright SI, McKay JK, Sharbel TF 2017. Mutation accumulation in an asexual relative of Arabidopsis. . PLOS Genet 13:1e1006550
    [Google Scholar]
  71. Lutes AA, Baumann DP, Neaves WB, Baumann P 2011. Laboratory synthesis of an independently reproducing vertebrate species. PNAS 108:249910–15
    [Google Scholar]
  72. Lutes AA, Neaves WB, Baumann DP, Wiegraebe W, Baumann P 2010. Sister chromosome pairing maintains heterozygosity in parthenogenetic lizards. Nature 464:7286283–86
    [Google Scholar]
  73. Lynch M, Walsh B. 2007. The Origins of Genome Architecture Oxford, UK: Oxford Univ. Press
  74. Mank JE. 2009. The W, X, Y and Z of sex-chromosome dosage compensation. Trends Genet 25:5226–33
    [Google Scholar]
  75. Mark Welch D, Meselson M 2000. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288:54691211–15
    [Google Scholar]
  76. Mau M, Lovell JT, Corral JM, Kiefer C, Koch MA et al. 2015. Hybrid apomicts trapped in the ecological niches of their sexual ancestors. PNAS 112:18E2357–65
    [Google Scholar]
  77. Maynard-Smith J. 1978. The Evolution of Sex Cambridge, UK: Cambridge Univ. Press
  78. McClintock B. 1984. The significance of responses of the genome to challenge. Science 226:4676792–801
    [Google Scholar]
  79. McElroy KE, Denton RD, Sharbrough J, Bankers L, Neiman M, Gibbs HL 2017. Genome expression balance in a triploid trihybrid vertebrate. Genome Biol. Evol. 9:4968–80
    [Google Scholar]
  80. Meirmans S, Strand R. 2010. Why are there so many theories for sex, and what do we do with them. J. Hered. 101:Suppl. 1S3–12
    [Google Scholar]
  81. Miller KL, Castañeda Rico S, Muletz-Wolz CR, Campana MG, McInerney N et al. 2019. Parthenogenesis in a captive Asian water dragon (Physignathus cocincinus) identified with novel microsatellites. PLOS ONE 14:6e0217489
    [Google Scholar]
  82. Moritz C. 1984. The origin and evolution of parthenogenesis in Heteronotia binoei (Gekkonidae). Chromosoma 89:2151–62
    [Google Scholar]
  83. Moritz C, McCallum H, Donnellan S, Roberts JD, Pettigrew JD 1991. Parasite loads in parthenogenetic and sexual lizards (Heteronotia binoei): support for the Red Queen hypothesis. Proc. R. Soc. B 244:1310145–49
    [Google Scholar]
  84. Moritz CC, Brown WM, Densmore LD 3rd, Wright JW, Vyas D et al. 1989. Genetic diversity and the dynamics of hybrid parthenogenesis in Cnemidophorus (Teiidae) and Heteronotia (Gekkonidae). Bull. N.Y. State Mus. 466:87–112
    [Google Scholar]
  85. Muller HJ. 1964. The relation of recombination to mutational advance. Mutat. Res. 106:2–9
    [Google Scholar]
  86. Murakami Y, Hayashi F. 2019. Molecular discrimination and phylogeographic patterns of clones of the parthenogenetic gecko Lepidodactylus lugubris in the Japanese Archipelago. Popul. Ecol. 61:3315–24
    [Google Scholar]
  87. Murphy RW, Fu J, Macculloch RD, Darevsky IS, Kupriyanova LA 2000. A fine line between sex and unisexuality: the phylogenetic constraints on parthenogenesis in lacertid lizards. Zool. J. Linn. Soc. 130:4527–49
    [Google Scholar]
  88. Neaves WB, Baumann P. 2011. Unisexual reproduction among vertebrates. Trends Genet 27:381–88
    [Google Scholar]
  89. Neiman M, Hehman G, Miller JT, Logsdon JM Jr., Taylor DR 2010. Accelerated mutation accumulation in asexual lineages of a freshwater snail. Mol. Biol. Evol. 27:4954–63
    [Google Scholar]
  90. Neiman M, Lively CM, Meirmans S 2017. Why sex? A pluralist approach revisited. Trends Ecol. Evol. 32:8589–600
    [Google Scholar]
  91. Newton AA, Schnittker RR, Yu Z, Munday SS, Baumann DP et al. 2016. Widespread failure to complete meiosis does not impair fecundity in parthenogenetic whiptail lizards. Development 143:234486–94
    [Google Scholar]
  92. Normark BB, Moran NA. 2000. Testing for the accumulation of deleterious mutations in asexual eukaryote genomes using molecular sequences. J. Nat. Hist. 34:91719–29
    [Google Scholar]
  93. Nuzhdin SV, Petrov DA. 2003. Transposable elements in clonal lineages: lethal hangover from sex. Biol. J. Linn. Soc. Lond. 79:133–41
    [Google Scholar]
  94. Orr HA. 1990. “Why polyploidy is rarer in animals than in plants” revisited. Am. Nat. 136:6759–70
    [Google Scholar]
  95. Otto SP. 2009. The evolutionary enigma of sex. Am. Nat. 174:Suppl. 1S1–14
    [Google Scholar]
  96. Otto SP, Barton NH. 1997. The evolution of recombination: removing the limits to natural selection. Genetics 147:2879–906
    [Google Scholar]
  97. Otto SP, Lenormand T. 2002. Evolution of sex: resolving the paradox of sex and recombination. Nat. Rev. Genet. 3:4252–61
    [Google Scholar]
  98. Pala I, Coelho MM, Schartl M 2008. Dosage compensation by gene-copy silencing in a triploid hybrid fish. Curr. Biol. 18:171344–48
    [Google Scholar]
  99. Parker DJ, Bast J, Jalvingh K, Dumas Z, Robinson-Rechavi M, Schwander T 2019. Sex-biased gene expression is repeatedly masculinized in asexual females. Nat. Commun. 10:14638
    [Google Scholar]
  100. Parsch J, Ellegren H. 2013. The evolutionary causes and consequences of sex-biased gene expression. Nat. Rev. Genet. 14:283–87
    [Google Scholar]
  101. Pellegrino KCM, Rodrigues MT, Harris DJ, Yonenaga-Yassuda Y, Sites JW Jr 2011. Molecular phylogeny, biogeography and insights into the origin of parthenogenesis in the Neotropical genus Leposoma (Squamata: Gymnophthalmidae): ancient links between the Atlantic Forest and Amazonia. Mol. Phylogenet. Evol. 61:2446–59
    [Google Scholar]
  102. Pellegrino KCM, Rodrigues MT, Yonenaga-Yassuda Y 1999. Chromosomal evolution in the Brazilian lizards of genus Leposoma (Squamata, Gymnophthalmidae) from Amazon and Atlantic rain forests: banding patterns and FISH of telomeric sequences. Hereditas 131:115–21
    [Google Scholar]
  103. Petrosyan V, Osipov F, Bobrov V, Dergunova N, Nazarenko E et al. 2019. Analysis of geographical distribution of the parthenogenetic rock lizard Darevskia armeniaca and its parental species (D. mixta, D. valentini) based on ecological modelling. Salamandra 55:3173–90
    [Google Scholar]
  104. Radtkey RR, Becker B, Miller RD, Riblet R, Case TJ 1996. Variation and evolution of class I MHC in sexual and parthenogenetic geckos. Proc. Biol. Sci. 263:13731023–32
    [Google Scholar]
  105. Radwan J, Babik W, Kaufman J, Lenz TL, Winternitz J 2020. Advances in the evolutionary understanding of MHC polymorphism. Trends Genet 36:4298–311
    [Google Scholar]
  106. Rapp RA, Wendel JF. 2005. Epigenetics and plant evolution. New Phytol 168:181–91
    [Google Scholar]
  107. Rauh NR, Schmidt A, Bormann J, Nigg EA, Mayer TU 2005. Calcium triggers exit from meiosis II by targeting the APC/C inhibitor XErp1 for degradation. Nature 437:70611048–52
    [Google Scholar]
  108. Ren L, Li W, Tao M, Qin Q, Luo J et al. 2016. Homoeologue expression insights into the basis of growth heterosis at the intersection of ploidy and hybridity in Cyprinidae. Sci. Rep. 6:27040
    [Google Scholar]
  109. Ren L, Tang C, Li W, Cui J, Tan X et al. 2017. Determination of dosage compensation and comparison of gene expression in a triploid hybrid fish. BMC Genom 18:138
    [Google Scholar]
  110. Renfree MB, Suzuki S, Kaneko-Ishino T 2013. The origin and evolution of genomic imprinting and viviparity in mammals. Philos. Trans. R. Soc. B 368:160920120151
    [Google Scholar]
  111. Runemark A, Trier CN, Eroukhmanoff F, Hermansen JS, Matschiner M et al. 2018. Variation and constraints in hybrid genome formation. Nat. Ecol. Evol. 2:3549–56
    [Google Scholar]
  112. Ryskov AP, Osipov FA, Omelchenko AV, Semyenova SK, Girnyk AE et al. 2017. The origin of multiple clones in the parthenogenetic lizard species Darevskia rostombekowi. . PLOS ONE 12:9e0185161
    [Google Scholar]
  113. Schaack S, Pritham EJ, Wolf A, Lynch M 2010. DNA transposon dynamics in populations of Daphnia pulex with and without sex. Proc. Biol. Sci. 277:16922381–87
    [Google Scholar]
  114. Schön I, Martens K, Dijk P 2009. Lost Sex: The Evolutionary Biology of Parthenogenesis Dordrecht, Neth.: Springer
  115. Sinclair EA, Pramuk JB, Bezy RL, Crandall KA, Sites JW Jr 2010. DNA evidence for nonhybrid origins of parthenogenesis in natural populations of vertebrates. Evolution 64:51346–57
    [Google Scholar]
  116. Sites JW, Reeder TW, Wiens JJ 2011. Phylogenetic insights on evolutionary novelties in lizards and snakes: sex, birth, bodies, niches, and venom. Annu. Rev. Ecol. Evol. Syst. 42:227–44
    [Google Scholar]
  117. Spangenberg V, Arakelyan M, Galoyan E, Matveevsky S, Petrosyan R et al. 2017. Reticulate evolution of the rock lizards: meiotic chromosome dynamics and spermatogenesis in diploid and triploid males of the genus Darevskia. . Genes 8:6149
    [Google Scholar]
  118. Strasburg JL, Kearney M. 2005. Phylogeography of sexual Heteronotia binoei (Gekkonidae) in the Australian arid zone: climatic cycling and repetitive hybridization. Mol. Ecol. 14:92755–72
    [Google Scholar]
  119. Strasburg JL, Kearney M, Moritz C, Templeton AR 2007. Combining phylogeography with distribution modeling: multiple Pleistocene range expansions in a parthenogenetic gecko from the Australian arid zone. PLOS ONE 2:8e760
    [Google Scholar]
  120. Tarkhnishvili D, Gavashelishvili A, Avaliani A, Murtskhvaladze M, Mumladze L 2010. Unisexual rock lizard might be outcompeting its bisexual progenitors in the Caucasus. Biol. J. Linn. Soc. Lond. 101:2447–60
    [Google Scholar]
  121. Uzzell T. 1970. Meiotic mechanisms of naturally occurring unisexual vertebrates. Am. Nat. 104:939433–45
    [Google Scholar]
  122. van der Kooi CJ, Schwander T 2014. On the fate of sexual traits under asexuality. Biol. Rev. Camb. Philos. Soc. 89:4805–19
    [Google Scholar]
  123. van Dijk EL, Jaszczyszyn Y, Naquin D, Thermes C 2018. The third revolution in sequencing technology. Trends Genet 34:9666–81
    [Google Scholar]
  124. Verhoeven KJF, Preite V. 2014. Epigenetic variation in asexually reproducing organisms. Evolution 68:3644–55
    [Google Scholar]
  125. Vicoso B. 2019. Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nat. Ecol. Evol. 3:121632–41
    [Google Scholar]
  126. Volobouev V, Pasteur G. 1988. Presumptive sex chromosomes of a unisexual homomorphic species of lizards. Lepidodactylus lugubris. Heredity 60:Part 3463–67
    [Google Scholar]
  127. Vrijenhoek RC. 1979. Factors affecting clonal diversity and coexistence. Am. Zool. 19:3787–97
    [Google Scholar]
  128. Vrijenhoek RC. 1984. Ecological differentiation among clones: the frozen niche variation model. Population Biology and Evolution K Wohrmann, V Loeschke 217–31 Berlin: Springer-Verlag
    [Google Scholar]
  129. Vrijenhoek RC, Parker ED. 2009. Geographical parthenogenesis: general purpose genotypes and frozen niche variation. See Schön et al. 2009 99–131
  130. Wang B, Tseng E, Baybayan P, Eng K, Regulski M et al. 2020. Variant phasing and haplotypic expression from long-read sequencing in maize. Commun. Biol. 3:178
    [Google Scholar]
  131. Warren WC, García-Pérez R, Xu S, Lampert KP, Chalopin D et al. 2018. Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly. Nat. Ecol. Evol. 2:4669–79
    [Google Scholar]
  132. Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R 2006. Parthenogenesis in Komodo dragons. Nature 444:71221021–22
    [Google Scholar]
  133. Wei X, Zhang J. 2018. The optimal mating distance resulting from heterosis and genetic incompatibility. Sci Adv 4:11 eaau5518
    [Google Scholar]
  134. Wendel JF. 2000. Genome evolution in polyploids. Plant Mol. Biol. 42:1225–49
    [Google Scholar]
  135. Yin D, Schwarz EM, Thomas CG, Felde RL, Korf IF et al. 2018. Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins. Science 359:637155–61
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-011720-114900
Loading
/content/journals/10.1146/annurev-ecolsys-011720-114900
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error