1932

Abstract

Evolutionary rates and strength of selection differ markedly between haploid and diploid genomes. Any genes expressed in a haploid state will be directly exposed to selection, whereas alleles in a diploid state may be partially or fully masked by a homologous allele. This difference may shape key evolutionary processes, including rates of adaptation and inbreeding depression, but also the evolution of sex chromosomes, heterochiasmy, and stable sex ratio biases. All diploid organisms carry haploid genomes, most notably the haploid genomes in gametes produced by every sexually reproducing eukaryote. Furthermore, haploid expression occurs in genes with monoallelic expression, in sex chromosomes, and in organelles, such as mitochondria and plastids. A comparison of evolutionary rates among these haploid genomes reveals striking parallels. Evidence suggests that haploid selection has the potential to shape evolution in predominantly diploid organisms, and taking advantage of the rapidly developing technologies, we are now in the position to quantify the importance of such selection on haploid genomes.

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2019-11-02
2024-10-06
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Literature Cited

  1. Alavioon G, Hotzy H, Nakhro K, Rudolf S, Scofield DG et al. 2017. Haploid selection within a single ejaculate increases offspring fitness. PNAS 114:8053–58
    [Google Scholar]
  2. Ardon F, Helms D, Sahin E, Bollwein H, Topfer-Petersen E, Waberski D 2008. Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo. Reproduction 135:4461–70
    [Google Scholar]
  3. Armbruster WS, Gobeille Rogers D 2004. Does pollen competition reduce the cost of inbreeding. Am. J. Bot. 91:111939–43
    [Google Scholar]
  4. Arnqvist G, Rowe L. 2005. Sexual Conflict Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  5. Aronen T, Nikkanen T, Harju A, Tiimonen H, Häggman H 2002. Pollen competition and seed-siring success in Picea abies. Theor. Appl. Genet 104:4638–42
    [Google Scholar]
  6. Arunkumar R, Josephs EB, Williamson RJ, Wright SI 2013. Pollen-specific, but not sperm-specific, genes show stronger purifying selection and higher rates of positive selection than sporophytic genes in Capsella grandiflora. Mol. Biol. Evol. 30:2475–86
    [Google Scholar]
  7. Bachtrog D, Mank JE, Peichel CL, Otto SP, Kirkpatrick M et al. 2014. Sex determination: why so many ways of doing it. PLOS Biol 12:e1001899
    [Google Scholar]
  8. Ballard JWO, Whitlock MC. 2004. The incomplete natural history of mitochondria. Mol. Ecol. 13:4729–44
    [Google Scholar]
  9. Barr CM, Neiman M, Taylor DR 2005. Inheritance and recombination of mitochondrial genomes in plants, fungi and animals: research review. New Phytol 168:139–50
    [Google Scholar]
  10. Birkhead TR, Møller AP. 1998. Sperm Competition and Sexual Selection London: Academic
    [Google Scholar]
  11. Borg M, Brownfield L, Twell D 2009. Male gametophyte development: a molecular perspective. J. Exp. Bot. 60:51465–78
    [Google Scholar]
  12. Borowsky R, Luk A, He X, Kim RS 2018. Unique sperm haplotypes are associated with phenotypically different sperm subpopulations in Astyanax fish. BMC Biol 16:72
    [Google Scholar]
  13. Brockdorff N, Turner BM. 2015. Dosage compensation in mammals. Cold Spring Harb. Perspect. Biol. 7:3a019406
    [Google Scholar]
  14. Caldwell KA, Handel MA. 1991. Protamine transcript sharing among postmeiotic spermatids. PNAS 88:2407–11
    [Google Scholar]
  15. Carré D, Sardet C. 1984. Fertilization and early development in Beroe ovata. Dev. Biol 105:188–95
    [Google Scholar]
  16. Charlesworth B. 1978. Model for evolution of Y-chromosomes and dosage compensation. PNAS 75:5618–22
    [Google Scholar]
  17. Charlesworth B. 1996. The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6:2149–62
    [Google Scholar]
  18. Charlesworth B, Charlesworth D. 1987. Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst. 18:237–68
    [Google Scholar]
  19. Charlesworth D, Charlesworth B. 1992. The effects of selection in the gametophytic stage on mutational load. Evolution 46:703–20
    [Google Scholar]
  20. Chess A. 2012. Mechanisms and consequences of widespread random monoallelic expression. Nat. Rev. Genet. 13:421–28
    [Google Scholar]
  21. Clarke HJ, Khan TN, Siddique KHM 2004. Pollen selection for chilling tolerance at hybridisation leads to improved chickpea cultivars. Euphytica 139:65–74
    [Google Scholar]
  22. Cohen J. 1967. Correlation between sperm “redundancy” and chiasma frequency. Nature 215:862–63
    [Google Scholar]
  23. Cohen J. 1973. Cross-overs, sperm redundancy and their close association. Heredity 31:408–13
    [Google Scholar]
  24. Crow JF, Kimura M. 1965. Evolution of sexual and asexual populations. Am. Nat. 99:439–50
    [Google Scholar]
  25. Crow JF, Kimura M. 1970. An Introduction to Population Genetics Theory New York: Harper & Row
    [Google Scholar]
  26. Day T, Bonduriansky R. 2004. Intralocus sexual conflict can drive the evolution of genomic imprinting. Genetics 167:1537–46
    [Google Scholar]
  27. de Vries J, Archibald JM 2018. Plastid autonomy versus nuclear control over plastid function. Plastid Genome Evolution S-M Chaw, RK Jansen 1–28 London Academic
    [Google Scholar]
  28. Dean R, Zimmer F, Mank JE 2014. The potential role of sexual conflict and sexual selection in shaping the genomic distribution of mito-nuclear genes. Genome Biol. Evol. 6:51096–104
    [Google Scholar]
  29. Domínguez E, Cuartero J, Fernández-Muñoz R 2005. Breeding tomato for pollen tolerance to low temperatures by gametophytic selection. Euphytica 142:253–63
    [Google Scholar]
  30. Dym M, Fawcett DW. 1971. Further observations on the numbers of spermatogonia, spermatocytes, and spermatids connected by intercellular bridges in the mammalian testis. Biol. Reprod. 4:2195–215
    [Google Scholar]
  31. Erickson RP. 1973. Haploid gene expression versus meiotic drive: the relevance of intercellular bridges during spermatogenesis. Nat. New Biol. 243:210–12
    [Google Scholar]
  32. Erickson RP. 1990. Post-meiotic gene expression. Trends Genet 6:8264–68
    [Google Scholar]
  33. Ewing E. 1977. Selection at the haploid and diploid phases: cyclical variation. Genetics 87:195–208
    [Google Scholar]
  34. Ezawa K, Innan H. 2013. Competition between the sperm of a single male can increase the evolutionary rate of haploid expressed genes. Genetics 194:3709–19
    [Google Scholar]
  35. Fitzpatrick JL, Baer B. 2011. Polyandry reduces sperm length variation in social insects. Evolution 65:103006–12
    [Google Scholar]
  36. Good JM, Nachman MW. 2005. Rates of protein evolution are positively correlated with developmental timing of expression during mouse spermatogenesis. Mol. Biol. Evol. 22:41044–52
    [Google Scholar]
  37. Good JM, Vanderpool D, Smith KL, Nachman MW 2011. Extraordinary sequence divergence at Tsga8, an X-linked gene involved in mouse spermiogenesis. Mol. Biol. Evol. 28:51675–86
    [Google Scholar]
  38. Gordo I, Charlesworth B. 2000. The degeneration of asexual haploid populations and the speed of Muller's ratchet. Genetics 154:31379–87
    [Google Scholar]
  39. Gossmann TI, Schmid MW, Grossniklaus U, Schmid KJ 2014. Selection-driven evolution of sex-biased genes is consistent with sexual selection in Arabidopsis thaliana. Mol. Biol. Evol 31:3574–83
    [Google Scholar]
  40. Gur Y, Breitbart H. 2006. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev 20:411–16
    [Google Scholar]
  41. Gur Y, Breitbart H. 2008. Protein synthesis in sperm: dialog between mitochondria and cytoplasm. Mol. Cell. Endocrinol. 282:1–245–55
    [Google Scholar]
  42. Haig D. 2000. The kinship theory of genomic imprinting. Annu. Rev. Ecol. Syst. 31:9–32
    [Google Scholar]
  43. Haig D, Bergstrom CT. 1995. Multiple mating, sperm competition and meiotic drive. J. Evol. Biol. 8:3265–82
    [Google Scholar]
  44. Haldane JBS. 1924. A mathematical theory of natural and artificial selection. Part I. Trans. Camb. Philos. Soc. 23:219–41
    [Google Scholar]
  45. Haldane JBS. 1932. The Causes of Evolution New York: Harper
    [Google Scholar]
  46. Hartl DL. 1977. Applications of meiotic drive in animal breeding and population control. Proceedings of the International Congress on Quantitative Genetics E Pollak, O Kempthorne, TB Bailey Jr. 63–88 Ames: Iowa State Univ. Press
    [Google Scholar]
  47. Hecht NB. 1998. Molecular mechanisms of male germ cell differentiation. BioEssays 20:7555–61
    [Google Scholar]
  48. Holt WV, Van Look KJW 2004. Concepts in sperm heterogeneity, sperm selection and sperm competition as biological foundations for laboratory tests of semen quality. Reproduction 127:527–35
    [Google Scholar]
  49. Honys D, Twell D. 2004. Transcriptome analyses of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85
    [Google Scholar]
  50. Hough J, Immler S, Barrett SCH, Otto SP 2013. Evolutionarily stable sex ratios and mutation load. Evolution 67:71915–25
    [Google Scholar]
  51. Hourcade JD, Pérez-Crespo M, Fernández-González R, Pintado B, Gutiérrez-Adán A 2010. Selection against spermatozoa with fragmented DNA after postovulatory mating depends on the type of damage. Reprod. Biol. Endocrinol. 8:9
    [Google Scholar]
  52. Immler S, Arnqvist G, Otto SP 2012. Ploidally antagonistic selection maintains stable genetic polymorphism. Evolution 66:155–65
    [Google Scholar]
  53. Immler S, Otto SP. 2014. Driven apart: the evolution of ploidy differences between the sexes under antagonistic selection. Am. Nat. 183:196–107
    [Google Scholar]
  54. Immler S, Otto SP. 2018. The evolutionary consequences of selection at the haploid gametic stage. Am. Nat. 192:2241–49
    [Google Scholar]
  55. Joseph SB, Kirkpatrick M. 2004. Haploid selection in animals. Trends Ecol. Evol. 19:11592–97
    [Google Scholar]
  56. Kanippayoor RL, Alpern JHM, Moehring AJ 2013. Protamines and spermatogenesis in Drosophila and Homo sapiens. Spermatogenesis 3:2e24376
    [Google Scholar]
  57. Kirkpatrick M 1994. The Evolution of Haploid-Diploid Life Cycles Lect. Math. Life Sci. 25 Providence, RI: Am. Math. Soc.
    [Google Scholar]
  58. Kondrashov AS, Crow JF. 1991. Haploidy or diploidy: Which is better. Nature 351:314–15
    [Google Scholar]
  59. Lankinen A, Maad J, Armbruster WS 2009. Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): One-donor crosses reveal heritability but no effect on sporophytic-offspring fitness. Ann. Bot. 103:9941–50
    [Google Scholar]
  60. Lenormand T. 2003. The evolution of sex dimorphism in recombination. Genetics 163:811–22
    [Google Scholar]
  61. Lenormand T, Dutheil J. 2005. Recombination difference between sexes: a role for haploid selection. PLOS Biol 3:3e63
    [Google Scholar]
  62. Lenz TL, Hafer N, Samonte IE, Yeates SE, Milinski M 2018. Cryptic haplotype-specific gamete selection yields offspring with optimal MHC immune genes: sperm selection for optimal immune genes. Evolution 72:112478–90
    [Google Scholar]
  63. Lindsley DL, Grell EH. 1969. Spermiogenesis without chromosomes in Drosophila melanogaster. Genetics 61:69–78
    [Google Scholar]
  64. Losdat S, Chang S-M, Reid JM 2014. Inbreeding depression in male gametic performance. J. Evol. Biol. 27:6992–1011
    [Google Scholar]
  65. Lu S, Zong C, Fan W, Yang M, Li J et al. 2012. Probing meiotic recombination and aneuploidy of single sperm cells by whole-genome sequencing. Science 338:61141627–30
    [Google Scholar]
  66. Lyon MF, Glenister PH, Hawker SG 1972. Do the H-2 and T-loci of the mouse have a function in the haploid phase of sperm. Nature 240:152–53
    [Google Scholar]
  67. Mable BK, Otto SP. 1998. The evolution of life cycles with haploid and diploid phases. BioEssays 20:453–62
    [Google Scholar]
  68. MacLaughlin J, Terner C. 1973. Ribonucleic acid synthesis by spermatozoa from the rat and hamster. Biochem. J. 133:4635–39
    [Google Scholar]
  69. Manning JT, Chamberlain AT. 1994. Sib competition and sperm competitiveness: an answer to ‘why so many sperms?’ and the recombination/sperm number correlation. Proc. R. Soc. B 256:177–82
    [Google Scholar]
  70. Mascarenhas JP. 1990. Gene activity during pollen development. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:317–38
    [Google Scholar]
  71. Miller D, Ostermeier GC. 2006. Towards a better understanding of RNA carriage by ejaculate spermatozoa. Hum. Reprod. Update 12:6757–67
    [Google Scholar]
  72. Mulcahy DL 1975. Gamete Competition in Plants and Animals: Proceedings of the Symposium on Gamete Competition in Plants and Animals Amsterdam: North-Holland
    [Google Scholar]
  73. Muller HJ, Settles F. 1927. The non-functioning of the genes in spermatozoa. Z. Indukt. Abstamm. Vererbungslehre 43:285–312
    [Google Scholar]
  74. Nadeau JH. 2017. Do gametes woo? Evidence for non-random unions at fertilization. Genetics 207:2369–87
    [Google Scholar]
  75. Orr HA, Otto SP. 1994. Does diploidy increase the rate of adaptation. Genetics 136:1475–80
    [Google Scholar]
  76. Otto SP, Scott MF, Immler S 2015. Evolution of haploid selection in predominantly diploid organisms. PNAS 112:15952–57
    [Google Scholar]
  77. Park C, Carrel L, Makova KD 2010. Strong purifying selection at genes escaping X chromosome inactivation. Mol. Biol. Evol. 27:112446–50
    [Google Scholar]
  78. Parker GA. 1993. Sperm competition games: sperm size and sperm number under adult control. Proc. R. Soc. B 253:245–54
    [Google Scholar]
  79. Parker GA, Begon ME. 1993. Sperm competition games: sperm size and number under gametic control. Proc. R. Soc. B 253:255–62
    [Google Scholar]
  80. Pitnick S, Dobler R, Hosken DJ 2009. Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria. Proc. R. Soc. B 276:4029–34
    [Google Scholar]
  81. Podlaha O, Webb DM, Tucker PK, Zhang J 2005. Positive selection for indel substitutions in the rodent sperm protein Catsper1. Mol. Biol. Evol. 22:91845–52
    [Google Scholar]
  82. Podlaha O, Zhang J. 2003. Positive selection on protein-length in the evolution of a primate sperm ion channel. PNAS 100:12241–46
    [Google Scholar]
  83. Premkumar E, Bhargava PM. 1972. Transcription and translation in bovine spermatozoa. Nat. New Biol. 240:100139–43
    [Google Scholar]
  84. Promerová M, Alavioon G, Tusso S, Burri R, Immler S 2017. No evidence for MHC class II-based non-random mating at the gametic haplotype in Atlantic salmon. Heredity 118:563–67
    [Google Scholar]
  85. Radzvilavicius AL, Hadjivasiliou Z, Pomiankowski A, Lane N 2016. Selection for mitochondrial quality drives evolution of the germline. PLOS Biol 14:12e2000410
    [Google Scholar]
  86. Ramm SA, Scharer L, Ehmcke J, Wistuba J 2014. Sperm competition and the evolution of spermatogenesis. Mol. Hum. Reprod. 20:121169–79
    [Google Scholar]
  87. Reed FA, Aquadro CF. 2006. Mutation, selection and the future of human evolution. Trends Genet 22:9479–84
    [Google Scholar]
  88. Reik W, Walter J. 2001. Genomic imprinting: parental influence on the genome. Nat. Rev. Genet. 2:121–32
    [Google Scholar]
  89. Ren X, Chen X, Wang Z, Wang D 2017. Is transcription in sperm stationary or dynamic. J. Reprod. Dev. 63:5439–43
    [Google Scholar]
  90. Romiguier J, Lourenco J, Gayral P, Faivre N, Weinert LA et al. 2014. Population genomics of eusocial insects: the costs of a vertebrate-like effective population size. J. Evol. Biol. 27:3593–603
    [Google Scholar]
  91. Rossignol R, Faustin B, Rocher C, Malgat M, Mazat J-P, Letellier T 2003. Mitochondrial threshold effects. Biochem. J. 370:3751–62
    [Google Scholar]
  92. Sandler G, Beaudry FEG, Barrett SCH, Wright SI 2018. The effects of haploid selection on Y chromosome evolution in two closely related dioecious plants. Evol. Lett. 2:4368–77
    [Google Scholar]
  93. Sari-Gorla M, Frova C. 1997. Pollen tube growth and pollen selection. Pollen Biotechnology for Crop Production and Improvement KR Shivanna, VK Sawhney 333–51 Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  94. Scott C, de Souza FF, Aristizabal VHV, Hethrington L, Krisp C et al. 2018. Proteomic profile of sex-sorted bull sperm evaluated by SWATH-MS analysis. Anim. Reprod. Sci. 198:121–28
    [Google Scholar]
  95. Scott MF, Osmond MM, Otto SP 2018. Haploid selection, sex ratio bias, and transitions between sex-determining systems. PLOS Biol 16:6e2005609
    [Google Scholar]
  96. Scott MF, Otto SP. 2017. Haploid selection favours suppressed recombination between sex chromosomes despite causing biased sex ratios. Genetics 207:1631–49
    [Google Scholar]
  97. Scudo FM. 1967. Selection on both haplo and diplophase. Genetics 56:693–704
    [Google Scholar]
  98. Sharp NP, Sandell L, James CG, Otto SP 2018. The genome-wide rate and spectrum of spontaneous mutations differ between haploid and diploid yeast. PNAS 115:E5046–55
    [Google Scholar]
  99. Shoubridge EA, Wai T. 2007. Mitochondrial DNA and the mammalian oocyte. Current Topics in Developmental Biology 77 JC St. John 87–111 San Diego, CA: Academic
    [Google Scholar]
  100. Singh ND, Koerich LB, Carvalho AB, Clark AG 2014. Positive and purifying selection on the Drosophila Y chromosome. Mol. Biol. Evol. 31:102612–23
    [Google Scholar]
  101. Singh ND, Larracuente AM, Clark AG 2008. Contrasting the efficacy of selection on the X and autosomes in Drosophila. Mol. Biol. Evol. 25:2454–67
    [Google Scholar]
  102. Snook RR, Hosken DJ, Karr TL 2011. The biology and evolution of polyspermy: insights from cellular and functional studies of sperm and centrosomal behavior in the fertilized egg. Reproduction 142:6779–92
    [Google Scholar]
  103. Snow AA, Spira TP. 1996. Pollen-tube competition and male fitness in Hibiscus moscheutos. Evolution 50:51866–70
    [Google Scholar]
  104. Spillane C, Schmid KJ, Laoueillé-Duprat S, Pien S, Escobar-Restrepo J-M et al. 2007. Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448:349–52
    [Google Scholar]
  105. Steger K. 1999. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat. Embryol. 199:6471–87
    [Google Scholar]
  106. Strasburger E. 1894. The periodic reduction of the number of the chromosomes in the life-history of living organisms. Ann. Bot. 8:281–316
    [Google Scholar]
  107. Strasburger E. 1905. Typische und allotypische Kernteilung. Ergebnisse und Erörterungen. Jahrb. Wiss. Bot. 42:1–71
    [Google Scholar]
  108. Swanson WJ, Vacquier VD. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137–44
    [Google Scholar]
  109. Walbot V, Evans MMS. 2003. Unique features of the plant life cycle and their consequences. Nat. Rev. Genet. 4:5369–79
    [Google Scholar]
  110. Wang J, Fan HC, Behr B, Quake SR 2012. Genome-wide single cell analysis of recombination activity and de novo mutation rates in human sperm. Cell 150:2402–12
    [Google Scholar]
  111. Wang S, Zhang L, Meyer E, Matz MV 2009. Construction of a high-resolution genetic linkage map and comparative genome analysis for the reef-building coral Acropora millepora. Genome Biol 10:11R126
    [Google Scholar]
  112. Ward WS. 2018. Organization of sperm DNA by the nuclear matrix. Am. J. Clin. Exp. Urol. 6:287–92
    [Google Scholar]
  113. Wedekind C, Chapuisat M, Macas E, Rülicke T 1996. Non-random fertilization in mice correlates with the MHC and something else. Heredity 77:400–9
    [Google Scholar]
  114. Wedekind C, Walker M, Portmann J, Cenni B, Muller R, Binz T 2004. MHC-linked susceptibility to a bacterial infection, but no MHC-linked cryptic female choice in whitefish. J. Evol. Biol. 17:11–18
    [Google Scholar]
  115. Xu S, Ackerman MS, Long H, Bright L, Spitze K et al. 2015. A male-specific genetic map of the microcrustacean Daphnia pulex based on single-sperm whole-genome sequencing. Genetics 201:131–38
    [Google Scholar]
  116. Zamir D, Vallejos EC. 1983. Temperature effects on haploid selection of tomato microspores and pollen grains. Pollen: Biology and Implications for Plant Breeding DL Mulcahy, E Ottaviano 335–42 New York: Elsevier
    [Google Scholar]
  117. Zheng Y, Deng X, Martin-DeLeon PA 2001. Lack of sharing of Spam1 (Ph-20) among mouse spermatids and transmission ratio distortion. Biol. Reprod. 64:61730–38
    [Google Scholar]
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