1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Ecology, Evolution, and Systematics
  4. Volume 53, 2022
  5. Article

Annual Review of Ecology, Evolution, and Systematics

Volume 53, 2022

Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies

Abstract

The ability to reproduce is the key trait that distinguishes living organisms from inorganic matter, and the strategies used to achieve successful reproduction are almost as diverse as the organisms themselves. In animals, the most widespread form of reproduction involves separate male and female sexes: Each sex produces haploid gametes via meiosis, and two gametes fuse to form a new diploid organism. In some cases, both parents contribute equally to the nuclear and cytoplasmic genomes of their offspring. However, such fully symmetric reproduction of both parents represents the extreme end of a continuum toward complete asymmetry, where offspring inherit their nuclear and cytoplasmic genomes from only one of the two parents. Asymmetries also occur with respect to the fate of maternally and paternally inherited genomes and which sex is affected by non-Mendelian inheritance. In this review, we describe the diversity of animal reproductive systems along different axes with a symmetry–asymmetry continuum and suggest evolutionary routes that may have led to increased levels of asymmetry.

Keyword(s): evolutionary genetics, haplodiploidy, meiosis, parthenogenesis, reproduction, sex chromosomes
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-021822-010659
2022-11-02
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/53/1/annurev-ecolsys-021822-010659.html?itemId=/content/journals/10.1146/annurev-ecolsys-021822-010659&mimeType=html&fmt=ahah

Literature Cited

  1. Adamson ML. 1989. Evolutionary biology of the Oxyurida (Namatoda): biofacies of a haplodiploid taxon. Adv. Parasitol. 28:175–228
     [Google Scholar]
  2. Ahmad SF, Martins C. 2019. The modern view of B chromosomes under the impact of high scale omics analyses. Cells 8:2156
     [Google Scholar]
  3. Akera T, Trimm E, Lampson MA. 2019. Molecular strategies of meiotic cheating by selfish centromeres. Cell 178:51132–44.e10
     [Google Scholar]
  4. Anderson N, Jaron KS, Hodson CN, Couger MB, Ševčík J et al. 2020. Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems. PNAS 11923e2122580119
  5. Archetti M. 2004. Loss of complementation and the logic of two-step meiosis. J. Evol. Biol. 17:51098–105
     [Google Scholar]
  6. Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP et al. 2014. Sex determination: why so many ways of doing it?. PLOS Biol 12:7e1001899
     [Google Scholar]
  7. Barraclough TG, Birky CW Jr., Burt A. 2003. Diversification in sexual and asexual organisms. Evolution 57:92166–72
     [Google Scholar]
  8. 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]
  9. Bell G. 1982. The Masterpiece of Nature Abingdon, UK: Routledge
  10. Bendall EE, Bagley RK, Sousa VC, Linnen CR. 2021. Faster-haplodiploid evolution under divergence-with-gene-flow: simulations and empirical data from pine-feeding hymenopterans. Mol. Ecol. 31:82348–66
     [Google Scholar]
  11. Benetta ED, Antoshechkin I, Yang T, Nguyen HQM, Ferree PM, Akbari OS. 2020. Genome elimination mediated by gene expression from a selfish chromosome. Sci. Adv. 6:14eaaz9808
     [Google Scholar]
  12. Beukeboom L, Vrijenhoek RC. 1998. Evolutionary genetics and ecology of sperm-dependent parthenogenesis. J. Evol. Biol. 11:6755–82
     [Google Scholar]
  13. Birky CW. 2001. The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models. Annu. Rev. Genet. 35:125–48
     [Google Scholar]
  14. Birky CW, Barraclough TG 2009. Asexual speciation. Lost Sex: The Evolutionary Biology of Parthenogenesis I Schön, K Martens, P Dijk 201–16 Dordrecht, Neth: Springer
     [Google Scholar]
  15. Blackman RL. 1985. Spermatogenesis in the aphid Amphorophora tuberculata (Homoptera, Aphididae). Chromosoma 92:5357–62
     [Google Scholar]
  16. Blackmon H, Hardy NB, Ross L 2015. The evolutionary dynamics of haplodiploidy: genome architecture and haploid viability. Evolution 69:112971–78
     [Google Scholar]
  17. Bongiorni S, Fiorenzo P, Pippoletti D, Prantera G. 2004. Inverted meiosis and meiotic drive in mealybugs. Chromosoma 112:7331–41
     [Google Scholar]
  18. Bongiorni S, Pugnali M, Volpi S, Bizzaro D, Singh PB, Prantera G. 2009. Epigenetic marks for chromosome imprinting during spermatogenesis in coccids. Chromosoma 118:4501–12
     [Google Scholar]
  19. Bressa MJ, Papeschi AG, Toloza AC. 2015. Cytogenetic features of human head and body lice (Phthiraptera: Pediculidae). J. Med. Entomol. 52:5918–24
     [Google Scholar]
  20. Brown SW. 1964. Automatic frequency response in evolution of male haploidy + other coccid chromosome systems. Genetics 49:5797–817
     [Google Scholar]
  21. Brown SW, Nur U. 1964. Heterochromatic chromosomes in coccids. Science 145:362130–36
     [Google Scholar]
  22. Brun LO, Stuart J, Gaudichon V, Aronstein K, French-Constant RH. 1995. Functional haplodiploidy: a mechanism for the spread of insecticide resistance in an important international insect pest. PNAS 92:219861–65
     [Google Scholar]
  23. Bull JJ. 1979. An advantage for the evolution of male haploidy and systems with similar genetic transmission. Heredity 43:3361–81
     [Google Scholar]
  24. Bull JJ, Cummings B. 1983. The Evolution of Sex Determining Mechanisms Menlo Park, CA: Benjamin Cummings
  25. Burt A, Trivers RL. 2006. Genes in Conflict Cambridge, MA: Harvard Univ. Press
  26. Cahan SH, Parker JD, Rissing SW, Johnson RA, Polony TS et al. 2002. Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc. R. Soc. B 269:15031871–77
     [Google Scholar]
  27. Cahan SH, Vinson SB. 2003. Reproductive division of labor between hybrid and nonhybrid offspring in a fire ant hybrid zone. Evolution 57:71562–70
     [Google Scholar]
  28. Camacho JPM 2005. B chromosomes. The Evolution of the Genome TR Gregory 223–86 Cambridge, MA: Academic
     [Google Scholar]
  29. Camacho JPM, Sharbel TF, Beukeboom LW. 2000. B-chromosome evolution. Philos. Trans. R. Soc. B 355:1394163–78
     [Google Scholar]
  30. Cameron S. 2014. How to sequence and annotate insect mitochondrial genomes for systematic and comparative genomics research. Syst. Entomol. 39:3400–11
     [Google Scholar]
  31. Carvalho AB. 2002. Origin and evolution of the Drosophila Y chromosome. Curr. Opin. Genet. Dev. 12:6664–68
     [Google Scholar]
  32. Charlesworth D, Willis JH. 2009. The genetics of inbreeding depression. Nat. Rev. Genet. 10:11783–96
     [Google Scholar]
  33. Chmielewska M, Dedukh D, Haczkiewicz K, Rozenblut-Kościsty B, Kaźmierczak M et al. 2018. The programmed DNA elimination and formation of micronuclei in germ line cells of the natural hybridogenetic water frog Pelophylax esculentus. Sci. Rep. 8:17870
     [Google Scholar]
  34. Couger MB, Roy SW, Anderson N, Gozashti L, Pirro S et al. 2021. Sex chromosome transformation and the origin of a male-specific X chromosome in the creeping vole. Science 372:6542592–600
     [Google Scholar]
  35. Crouse HV, Brown A, Mumford BC. 1971. L-chromosome inheritance and the problem of chromosome “imprinting” in Sciara (Sciaridae, Diptera). Chromosoma 34:3324–39
     [Google Scholar]
  36. Cui Y, Wang W, Ma L, Jie J, Zhang Y et al. 2018. New locus reveals the genetic architecture of sex reversal in the Chinese tongue sole (Cynoglossus semilaevis). Heredity 121:4319–26
     [Google Scholar]
  37. Dallai R, Fanciulli PP, Frati F. 1999. Chromosome elimination and sex determination in springtails (Insecta, Collembola). J. Exp. Zool. 285:3215–25
     [Google Scholar]
  38. de la Filia AG, Andrewes S, Clark JM, Ross L. 2017. The unusual reproductive system of head and body lice (Pediculus humanus). Med. Vet. Entomol. 32:226–34
     [Google Scholar]
  39. de la Filia AG, Bain SA, Ross L 2015. Haplodiploidy and the reproductive ecology of Arthropods. Curr. Opin. Insect Sci. 9:36–43
     [Google Scholar]
  40. de la Filia AG, Mongue AJ, Dorrens J, Lemon H, Laetsch DR, Ross L 2021. Males that silence their father's genes: genomic imprinting of a complete haploid genome. Mol. Biol. Evol. 38:62566–81
     [Google Scholar]
  41. Engelstädter J. 2008. Constraints on the evolution of asexual reproduction. BioEssays 30:11–121138–50
     [Google Scholar]
  42. Engelstädter J. 2017. Asexual but not clonal: evolutionary processes in automictic populations. Genetics 206:2993–1009
     [Google Scholar]
  43. Escriba MC, Goday C. 2013. Histone H3 phosphorylation and elimination of paternal X chromosomes at early cleavages in sciarid flies. J. Cell Sci. 126:143214–22
     [Google Scholar]
  44. Ferree PM, Aldrich JC, Jing XA, Norwood CT, Van Schaick MR et al. 2019. Spermatogenesis in haploid males of the jewel wasp Nasonia vitripennis. Sci. Rep. 9:112194
     [Google Scholar]
  45. Fournier D, Estoup A, Orivel J, Foucaud J, Jourdan H et al. 2005. Clonal reproduction by males and females in the little fire ant. Nature 435:70461230–34
     [Google Scholar]
  46. Fraïsse C, Picard MAL, Vicoso B. 2017. The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W. Nat. Commun. 8:11486
     [Google Scholar]
  47. Gardner A, Ross L. 2014. Mating ecology explains patterns of genome elimination. Ecol. Lett. 17:121602–12
     [Google Scholar]
  48. Gerbi SA. 1986. Unusual chromosome movements in sciarid flies. Germ Line—Soma Differentiation W Hennig 71–104 Berlin: Springer
     [Google Scholar]
  49. Gerstein A, Cleathero L, Mandegar M, Otto S 2011. Haploids adapt faster than diploids across a range of environments. J. Evol. Biol. 24:3531–40
     [Google Scholar]
  50. Gibson JR, Chippindale AK, Rice WR. 2002. The X chromosome is a hot spot for sexually antagonistic fitness variation. Proc. R. Soc. B 269:1490499–505
     [Google Scholar]
  51. Goday C, Esteban MR. 2001. Chromosome elimination in sciarid flies. BioEssays 23:3242–50
     [Google Scholar]
  52. Goday C, Pigozzi MI. 2010. Heterochromatin and histone modifications in the germline-restricted chromosome of the zebra finch undergoing elimination during spermatogenesis. Chromosoma 119:3325–36
     [Google Scholar]
  53. Greiner S, Sobanski J, Bock R. 2015. Why are most organelle genomes transmitted maternally?. BioEssays 37:180–94
     [Google Scholar]
  54. Grosmaire M, Launay C, Siegwald M, Brugière T, Estrada-Virrueta L et al. 2019. Males as somatic investment in a parthenogenetic nematode. Science 363:64321210–13
     [Google Scholar]
  55. Hadjivasiliou Z, Pomiankowski A. 2016. Gamete signalling underlies the evolution of mating types and their number. Philos. Trans. R. Soc. B 371:170620150531
     [Google Scholar]
  56. Haig D. 1993. The evolution of unusual chromosomal systems in sciarid flies: intragenomic conflict and the sex ratio. J. Evol. Biol. 6:2249–61
     [Google Scholar]
  57. Hamilton PT, Hodson CN, Curtis CI, Perlman SJ. 2018. Genetics and genomics of an unusual selfish sex ratio distortion in an insect. Curr. Biol. 28:233864–70.e4
     [Google Scholar]
  58. Hansson B. 2019. On the origin and evolution of germline chromosomes in songbirds. PNAS 116:2411570–72
     [Google Scholar]
  59. Hartl DL, Brown SW. 1970. The origin of male haploid genetic systems and their expected sex ratio. Theor. . Popul. Biol. 1:2165–90
     [Google Scholar]
  60. Hedrick PW, Parker JD. 1997. Evolutionary genetics and genetic variation of haplodiploids and X-linked genes. Annu. Rev. Ecol. Syst. 28:55–83
     [Google Scholar]
  61. Heppich S. 1978. Hybridogenesis in Ranaesculenta: C-band karyotypes of Rana ridibunda, Rana lessonae and Rana esculenta. J. Zool. Syst. Evol. Res. 16:127–39
     [Google Scholar]
  62. Herbette M, Wei X, Chang C-H, Larracuente AM, Loppin B, Dubruille R. 2021. Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system. PLOS Genet 17:7e1009662
     [Google Scholar]
  63. Hitchcock TJ, Gardner A, Ross L. 2021. Sexual antagonism in haplodiploids. Evolution 76:2292–309
     [Google Scholar]
  64. Hodson CN, Hamilton PT, Dilworth D, Nelson CJ, Curtis CI, Perlman SJ. 2017. Paternal genome elimination in Liposcelis booklice (Insecta: Psocodea). Genetics 206:21091–100
     [Google Scholar]
  65. Hodson CN, Jaron KS, Gerbi S, Ross L 2021. Evolution of gene-rich germline restricted chromosomes in black-winged fungus gnats through introgression (Diptera: Sciaridae). PLOS Biol 20:2e3001559
     [Google Scholar]
  66. Hodson CN, Perlman SJ. 2019. Population biology of a selfish sex ratio distorting element in a booklouse (Psocodea: Liposcelis). J. Evol. Biol. 32:8825–32
     [Google Scholar]
  67. Hodson CN, Ross L. 2021. Evolutionary perspectives on germline-restricted chromosomes in flies (Diptera). Genome Biol. Evol. 13:6evab072
     [Google Scholar]
  68. Hoeh WR, Blakley KH, Brown WM. 1991. Heteroplasmy suggests limited biparental inheritance of Mytilus mitochondrial DNA. Science 251:50001488–90
     [Google Scholar]
  69. Houben A. 2017. B chromosomes—a matter of chromosome drive. Front. Plant Sci. 8:210
     [Google Scholar]
  70. Hughes-Schrader S. 1925. Cytology of hermaphroditism in Icerya purchasi (Coccidae). Cell Tissue Res 2:2264–90
     [Google Scholar]
  71. Hunter MS, Nur U, Werren JH. 1993. Origin of males by genome loss in an autoparasitoid wasp. Heredity 70:2162–71
     [Google Scholar]
  72. Hurst GDD, Werren JH. 2001. The role of selfish genetic elements in eukaryotic evolution. Nat. Rev. Genet. 2:8597–606
     [Google Scholar]
  73. Hurst L. 1995. Selfish genetic elements and their role in evolution: the evolution of sex and some of what that entails. Philos. Trans. R. Soc. B 349:1329321–32
     [Google Scholar]
  74. Irie N, Satoh N, Kuratani S. 2018. The phylum Vertebrata: a case for zoological recognition. Zool. Lett. 4:132
     [Google Scholar]
  75. Ishibashi R, Ookubo K, Aoki M, Utaki M, Komaru A, Kawamura K. 2003. Androgenetic reproduction in a freshwater diploid clam Corbicula fluminea (Bivalvia: Corbiculidae). Zool. Sci. 20:6727–32
     [Google Scholar]
  76. Jalvingh K, Bast J, Schwander T 2016. Sex, evolution and maintenance of. Encyclopedia of Evolutionary Biology RM Kliman 89–97 Oxford, UK: Academic
     [Google Scholar]
  77. Jarne P, Auld JR. 2006. Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals. Evolution 60:91816–24
     [Google Scholar]
  78. Jaron KS, Bast J, Nowell RW, Ranallo-Benavidez TR, Robinson-Rechavi M, Schwander T. 2021a. Genomic features of parthenogenetic animals. J. Hered. 112:119–33
     [Google Scholar]
  79. Jaron KS, Hodson CN, Ellers J, Baird SJ, Ross L. 2021b. Genomic evidence of paternal genome elimination in the globular springtail Allacma fusca. Genetics In press. https://doi.org/10.1093/genetics/iyac117
    [Crossref]
  80. Jaron KS, Parker DJ, Anselmetti Y, Van PT, Bast J et al. 2021c. Convergent consequences of parthenogenesis on stick insect genomes. Sci. Adv. 8:8eabg3842
     [Google Scholar]
  81. Jones RN. 1991. B-chromosome drive. Am. Nat. 137:3430–42
     [Google Scholar]
  82. Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D. 2002. Genetic determination of the queen caste in an ant hybrid zone. PNAS 99:128157–60
     [Google Scholar]
  83. Kimura-Kawaguchi MR, Horita M, Abe S, Arai K, Kawata M, Munehara H. 2014. Identification of hemiclonal reproduction in three species of hexagrammos marine reef fishes. J. Fish Biol. 85:2189–209
     [Google Scholar]
  84. Kinsella CM, Ruiz-Ruano FJ, Dion-Côté A-M, Charles AJ, Gossmann TI et al. 2019. Programmed DNA elimination of germline development genes in songbirds. Nat. Commun. 10:15468
     [Google Scholar]
  85. Klein K, Kokko H, ten Brink H. 2021. Disentangling verbal arguments: intralocus sexual conflict in haplodiploids. Am. Nat. 198:6678–93
     [Google Scholar]
  86. Kobayashi K, Hasegawa E, Ohkawara K. 2008. Clonal reproduction by males of the ant Vollenhovia emeryi (Wheeler). Entomol. Sci. 11:167–72
     [Google Scholar]
  87. Komaru A, Kawagishi T, Konishi K. 1998. Cytological evidence of spontaneous androgenesis in the freshwater clam Corbicula leana Prime. Dev. Genes Evol. 208:146–50
     [Google Scholar]
  88. Kruger AN, Mueller JL. 2021. Mechanisms of meiotic drive in symmetric and asymmetric meiosis. Cell. Mol. Life Sci. 78:73205–18
     [Google Scholar]
  89. Kuhn A, Darras H, Paknia O, Aron S 2020. Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants. Mol. Ecol. 29:3549–64
     [Google Scholar]
  90. Ladoukakis ED, Zouros E. 2017. Evolution and inheritance of animal mitochondrial DNA: rules and exceptions. J. Biol. Res.-Thessalon. 24:12
     [Google Scholar]
  91. Lehtonen J, Schmidt DJ, Heubel K, Kokko H. 2013. Evolutionary and ecological implications of sexual parasitism. Trends Ecol. Evol. 28:5297–306
     [Google Scholar]
  92. Leniaud L, Darras H, Boulay R, Aron S 2012. Social hybridogenesis in the clonal ant Cataglyphis hispanica. Curr. Biol. 22:131188–93
     [Google Scholar]
  93. Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR. 2016. Evolutionary mysteries in meiosis. Philos. Trans. R. Soc. B 371:170620160001
     [Google Scholar]
  94. Li X-Y, Zhang Q-Y, Zhang J, Zhou L, Li Z et al. 2016. Extra microchromosomes play male determination role in polyploid gibel carp. Genetics 203:31415–24
     [Google Scholar]
  95. Lohse K, Ross L. 2015. What haplodiploids can teach us about hybridization and speciation. Mol. Ecol. 24:205075–77
     [Google Scholar]
  96. Majtánová Z, Dedukh D, Choleva L, Adams M, Ráb P et al. 2021. Uniparental genome elimination in Australian carp gudgeons. Genome Biol. Evol. 13:6evab030
     [Google Scholar]
  97. Mantovani B, Scali V. 1992. Hybridogenesis and androgenesis in the stick-insect Bacillus rossius-grandii benazzii (Insecta, Phasmatodea). Evolution 46:3783–96
     [Google Scholar]
  98. Marescalchi O, Scali V. 2001. New DAPI and FISH findings on egg maturation processes in related hybridogenetic and parthenogenetic Bacillus hybrids (insecta, phasmatodea). Mol. Reprod. Dev. 60:2270–76
     [Google Scholar]
  99. Marimuthu MPA, Maruthachalam R, Bondada R, Kuppu S, Tan EH et al. 2021. Epigenetically mismatched parental centromeres trigger genome elimination in hybrids. Sci. Adv. 7:47eabk1151
     [Google Scholar]
  100. Marlétaz F, Peijnenburg KTCA, Goto T, Satoh N, Rokhsar DS. 2019. A new spiralian phylogeny places the enigmatic arrow worms among gnathiferans. Curr. Biol. 29:2312–18.e3
     [Google Scholar]
  101. Maynard-Smith J. 1978. The Evolution of Sex Cambridge, UK: Cambridge Univ. Press
  102. McKone MJ, Halpern SL. 2003. The evolution of androgenesis. Am. Nat. 161:4641–56
     [Google Scholar]
  103. McMeniman CJ, Barker SC. 2005. Transmission ratio distortion in the human body louse, Pediculus humanus (Insecta: Phthiraptera). Heredity 96:163–68
     [Google Scholar]
  104. Metz CW. 1938. Chromosome behavior, inheritance and sex determination in Sciara. Am. Nat. 72:485–520
     [Google Scholar]
  105. Misof B, Liu S, Meusemann K, Peters RS, Donath A et al. 2014. Phylogenomics resolves the timing and pattern of insect evolution. Science 346:6210763–67
     [Google Scholar]
  106. Mockford EL. 1971. Parthenogenesis in Psocids (Insecta: Psocoptera). Am. Zool. 11:2327–39
     [Google Scholar]
  107. Molinier C, Lenormand T, Haag CR. 2021. No support for a meiosis suppressor in Daphnia pulex: Comparison of linkage maps reveals normal recombination in males of obligate parthenogenetic lineages. bioRxiv 2021.12.09.471908. https://doi.org/10.1101/2021.12.09.471908
    [Crossref]
  108. Mongue AJ, Michaelides S, Coombe O, Tena A, Kim D-S et al. 2021. Sex, males, and hermaphrodites in the scale insect Icerya purchasi. Evolution 75:112972–83
     [Google Scholar]
  109. Mullon C, Pomiankowski A, Reuter M. 2012. The effects of selection and genetic drift on the genomic distribution of sexually antagonistic alleles. Evolution 66:123743–53
     [Google Scholar]
  110. Neiman M, Sharbel TF, Schwander T. 2014. Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. J. Evol. Biol. 27:71346–59
     [Google Scholar]
  111. Nokkala S, Grozeva S, Kuznetsova V, Maryanska-Nadachowska A. 2003. The origin of the achiasmatic XY sex chromosome system in Cacopsylla peregrina (Frst.) (Psylloidea, Homoptera). Genetica 119:3327–32
     [Google Scholar]
  112. Norman V, Darras H, Tranter C, Aron S, Hughes WO 2016. Cryptic lineages hybridize for worker production in the harvester ant Messor barbarus. Biol. Lett. 12:1120160542
     [Google Scholar]
  113. Normark BB. 2003. The evolution of alternative genetic systems in insects. Annu. Rev. Entomol. 48:397–423
     [Google Scholar]
  114. Normark BB. 2004. Haplodiploidy as an outcome of coevolution between male-killing cytoplasmic elements and their hosts. Evolution 58:4790–98
     [Google Scholar]
  115. Normark BB. 2006. Perspective: maternal kin groups and the origins of asymmetric genetic systems—genomic imprinting, haplodiploidy, and parthenogenesis. Evolution 60:4631–42
     [Google Scholar]
  116. Norton RA, Kethley JB, Johnston DE, O'Connor BM. 1993. Phylogenetic perspectives on genetic systems and reproductive modes of mites. Evolution and Diversity of Sex Ratio in Insects and Mites D Wrensch, MA Ebbert 8–99 Boca Raton, FL: Chapman & Hall
     [Google Scholar]
  117. Nur U. 1990. Heterochromatization and euchromatization of whole genomes in scale insects (Coccoidea, Homoptera). Dev. Suppl. 1990:29–34
     [Google Scholar]
  118. Nur U, Werren JH, Eickbush DG, Burke WD, Eickbush TH. 1988. A ‘selfish’ B chromosome that enhances its transmission by eliminating the paternal genome. Science 240:4851512–14
     [Google Scholar]
  119. Ohkawara K, Nakayama M, Satoh A, Trindl A, Heinze J. 2006. Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. Biol. Lett. 2:3359–63
     [Google Scholar]
  120. Otto SP. 2021. Selective interference and the evolution of sex. J. Hered. 112:19–18
     [Google Scholar]
  121. Otto SP, Jarne P. 2001. Haploids – hapless or happening?. Science 292:55262441–43
     [Google Scholar]
  122. Pardo MC, López-León MD, Cabrero J, Camacho JPM. 1994. Transmission analysis of mitotically unstable B chromosomes in Locusta migratoria. Genome 37:61027–34
     [Google Scholar]
  123. 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]
  124. Parker GA, Baker RR, Smith VGF. 1972. The origin and evolution of gamete dimorphism and the male-female phenomenon. J. Theor. Biol. 36:3529–53
     [Google Scholar]
  125. Patten MM, Carioscia SA, Linnen CR. 2015. Biased introgression of mitochondrial and nuclear genes: a comparison of diploid and haplodiploid systems. Mol. Ecol. 24:205200–10
     [Google Scholar]
  126. Pearcy M, Aron S, Doums C, Keller L 2004. Conditional use of sex and parthenogenesis for worker and queen production in ants. Science 306:57021780–83
     [Google Scholar]
  127. Pearcy M, Goodisman MAD, Keller L. 2011. Sib mating without inbreeding in the longhorn crazy ant. Proc. R. Soc. B 278:17182677–81
     [Google Scholar]
  128. Pei Y, Forstmeier W, Ruiz-Ruano FJ, Mueller JC, Cabrero J et al. 2022. Occasional paternal inheritance of the germline-restricted chromosome in songbirds. PNAS 119:4e2103960119
     [Google Scholar]
  129. Pigozzi MI, Solari AJ. 2005. The germ-line-restricted chromosome in the zebra finch: recombination in females and elimination in males. Chromosoma 114:6403–9
     [Google Scholar]
  130. Pollock DA, Normark BB. 2002. The life cycle of Micromalthus debilisLeConte (1878) (Coleoptera: Archostemata: Micromalthidae): historical review and evolutionary perspective. J. Zool. Syst. Evol. Res. 40:2105–12
     [Google Scholar]
  131. Rice WR. 1984. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38:4735–42
     [Google Scholar]
  132. Romanenko SA, Smorkatcheva AV, Kovalskaya YM, Prokopov DY, Lemskaya NA et al. 2020. Complex structure of Lasiopodomys mandarinus vinogradovi sex chromosomes, sex determination, and intraspecific autosomal polymorphism. Genes 11:4374
     [Google Scholar]
  133. Romiguier J, Fournier A, Yek SH, Keller L. 2017. Convergent evolution of social hybridogenesis in Messor harvester ants. Mol. Ecol. 26:41108–17
     [Google Scholar]
  134. Ross L, Davies NG, Gardner A. 2019. How to make a haploid male. Evol. Lett. 3:2173–84
     [Google Scholar]
  135. Ross L, Pen I, Shuker DM 2010. Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems. Biol. Rev. 85:4807–28
     [Google Scholar]
  136. Royer M. 1975. Hermaphroditism in insects: studies on Icerya purchasi. Intersexuality in the Animal Kingdom R Reinboth 135–45 Berlin: Springer
     [Google Scholar]
  137. Saunders PA, Perez J, Ronce O, Veyrunes F. 2022. Multiple sex chromosome drivers in a mammal with three sex chromosomes. Curr. Biol. 32:92001–10.e3
     [Google Scholar]
  138. Schultz RJ. 1969. Hybridization, unisexuality, and polyploidy in the teleost Poeciliopsis (Poeciliidae) and other vertebrates. Am. Nat. 103:934605–19
     [Google Scholar]
  139. Schwander T, Crespi BJ. 2009. Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Mol. Ecol. 18:128–42
     [Google Scholar]
  140. Schwander T, Oldroyd BP. 2016. Androgenesis: where males hijack eggs to clone themselves. Philos. Trans. R. Soc. B 371:170620150534
     [Google Scholar]
  141. Schwander T, Vuilleumier S, Dubman J, Crespi BJ. 2010. Positive feedback in the transition from sexual reproduction to parthenogenesis. Proc. R. Soc. B 277:16861435–42
     [Google Scholar]
  142. Shao R, Kirkness EF, Barker SC. 2009. The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus. Genome Res 19:5904–12
     [Google Scholar]
  143. Skibinski DOF, Gallagher C, Beynon CM. 1994a. Mitochondrial DNA inheritance. Nature 368:6474817–18
     [Google Scholar]
  144. Skibinski DOF, Gallagher C, Beynon CM. 1994b. Sex-limited mitochondrial-DNA transmission in the marine mussel Mytilus edulis. Genetics 138:3801–9
     [Google Scholar]
  145. Smith NGC. 2000. The evolution of haplodiploidy under inbreeding. Heredity 84:2186–92
     [Google Scholar]
  146. Suomalainen E, Saura A, Lokki J. 1987. Cytology and Evolution in Parthenogenesis Boca Raton, FL: CRC Press
  147. Tandonnet S, Farrell MC, Koutsovoulos GD, Blaxter ML, Parihar M et al. 2018. Sex- and gamete-specific patterns of X chromosome segregation in a trioecious nematode. Curr. Biol. 28:193–99.e3
     [Google Scholar]
  148. Templeton AR 1982. The prophecies of parthenogenesis. Evolution and Genetics of Life Histories H Dingle, JP Hegmann 75–101 New York: Springer
     [Google Scholar]
  149. Tinti F, Scali V. 1992. Genome exclusion and gametic DAPI-DNA content in the hybridogenetic Bacillus rossius-grandii benazzii complex (Insecta Phasmatodea). Mol. Reprod. Dev. 33:3235–42
     [Google Scholar]
  150. Tinti F, Scali V. 1995. Allozymic and cytological evidence for hemiclonal, all-paternal, and mosaic offspring of the hybridogenetic stick insect Bacillus rossius-grandii grandii. J. Exp. Zool. 273:2149–59
     [Google Scholar]
  151. van der Kooi CJ, Matthey-Doret C, Schwander T. 2017. Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evol. Lett. 1:6304–16
     [Google Scholar]
  152. Vea IM, de la Filia AG, Jaron KS, Mongue AJ, Ruiz-Ruano FJ et al. 2021. The B chromosome of Pseudococcus viburni: a selfish chromosome that exploits whole-genome meiotic drive. bioRxiv 2021.08.30.458195. https://doi.org/10.1101/2021.08.30.458195
    [Crossref]
  153. Vicoso B, Bachtrog D. 2015. Numerous transitions of sex chromosomes in Diptera. PLOS Biol 13:4e1002078
     [Google Scholar]
  154. Vicoso B, Charlesworth B. 2009. Effective population size and the faster-X effect: an extended model. Evolution 63:92413–26
     [Google Scholar]
  155. Volny VP, Gordon DM. 2002. Genetic basis for queen-worker dimorphism in a social insect. PNAS 99:96108–11
     [Google Scholar]
  156. Vrijenhoek RC 1989. Genetic and ecological constraints on the origins and establishment of unisexual vertebrates. Evolution and Ecology of Unisexual Vertebrates RM Dawley, JP Bogart 24–31 Albany, NY: N. Y. State Mus:.
     [Google Scholar]
  157. Wallace RL, Snell TW, Ricci C, Nogrady T. 1993. Rotifera, Part 1: Biology, Ecology and Systematics Kerkwerve, Neth.: Backhuys
  158. Wang J, Davis RE. 2014. Programmed DNA elimination in multicellular organisms. Curr. Opin. Genet. Dev. 27:26–34
     [Google Scholar]
  159. Werren JH. 1993. The evolution of inbreeding in haplodiploid organisms. The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives NW Thornhill 42–59 Chicago: Univ. Chicago Press
     [Google Scholar]
  160. Werren JH, Baldo L, Clark M. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6:741–51
     [Google Scholar]
  161. White MJD. 1973. Animal Cytology and Evolution London: Cambridge Univ. Press
  162. Williams GC. 1975. Sex and Evolution. Princeton, NJ: Princeton Univ. Press
  163. Wilson ACC, Sunnucks P, Hales DF. 1997. Random loss of X chromosome at male determination in an aphid, Sitobion near fragariae, detected using an X-linked polymorphic microsatellite marker. Genet. Res. 69:3233–36
     [Google Scholar]
  164. Wright S. 1931. Evolution in mendelian populations. Genetics 16:97–159
     [Google Scholar]
  165. Xu J. 2005. The inheritance of organelle genes and genomes: patterns and mechanisms. Genome 48:6951–58
     [Google Scholar]
  166. Zouros E, Ball AO, Saavedra C, Freeman KR. 1994. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. PNAS 91:167463–67
     [Google Scholar]
  167. Zouros E, Freeman KR, Ball AO, Pogson GH. 1992. Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine mussel Mytilus. Nature 359:6394412–14
     [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-021822-010659
Loading
Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies
Annual Review of Ecology, Evolution, and Systematics 53, 1 (2022); https://doi.org/10.1146/annurev-ecolsys-021822-010659
/content/journals/10.1146/annurev-ecolsys-021822-010659
/content/journals/10.1146/annurev-ecolsys-021822-010659
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

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