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Issue: Vol. 43 No. 1: 30 June 2021
Type: Article
Published: 2021-06-30
DOI: 10.11646/bde.43.1.11
Page range: 133–149
Abstract views: 534
PDF downloaded: 416

Does degeneration or genetic conflict shape gene content on UV sex chromosomes?

Department of Biology, University of Florida, Gainesville, FL, USA; Department of Crop, Soil, and Environmental Sciences, Auburn University, Auburn, AL, USA; HudsonAlpha Institute for Biotechnology, Huntsville, AL, USA
Department of Biology, University of Florida, Gainesville, FL, USA
Department of Biology, University of Florida, Gainesville, FL, USA
UV sex chromosomes bryophytes algae genetic conflict speciation

Abstract

Studies of sex chromosomes have played a central role in understanding the consequences of suppressed recombination and sex-specific inheritance among several genomic phenomena. However, we argue that these efforts will benefit from a more rigorous examination of haploid UV sex chromosome systems, in which both the female-limited (U) and male-limited (V) experience suppressed recombination and sex-limited inheritance, and both are transcriptionally active in the haploid and diploid states. We review the life cycle differences that generate UV sex chromosomes and genomic data showing that ancient UV systems have evolved independently in many eukaryotic groups, but gene movement on and off the sex chromosomes, and potentially degeneration continue to shape the current gene content of the U and V chromosomes. Although both theory and empirical data show that the evolution of UV sex chromosomes is shaped by many of the same processes that govern diploid sex chromosome systems, we highlight how the symmetrical inheritance between the UV chromosomes provide an important test of sex-limited inheritance in shaping genome architecture. We conclude by examining how genetic conflict (over sexual dimorphism, transmission-ratio distortion, or parent-offspring conflict) may drive gene gain on UV sex chromosomes, and highlight the role of breeding system in governing the action of these processes. Collectively these observations demonstrate the potential for evolutionary genomic analyses of varied UV sex chromosome systems, combined with natural history studies, to understand how genetic conflict shapes sex chromosome gene content.

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References

  1. Ahmed, S., Cock, J.M., Pessia, E., Luthringer, R., Cormier, A., Robuchon, M., Sterck, L., Peters, A.F., Dittami, S.M., Corre, E., Valero, M., Aury, J.-M., Roze, D., Van de Peer, Y., Bothwell, J., Marais, G.A.B. & Coelho, S.M. (2014) A haploid system of sex determination in the brown alga Ectocarpus sp. Current biology 24 (17): 1945–1957. https://doi.org/10.1016/j.cub.2014.07.042

  2. Akagi, T., Henry, I.M., Tao, R. & Comai, L. (2014) A Y-chromosome–encoded small RNA acts as a sex determinant in persimmons. Science 346 (6209): 646–650. https://doi.org/10.1126/science.1257225

  3. Allen, C.E. (1917) A chromosome difference correlated with sex differences in sphærocarpos. Science 46 (1193): 466–467. https://doi.org/10.1126/science.46.1193.466

  4. Allen, C.E. (1945) The genetics of bryophytes. II. The Botanical review; interpreting botanical progress 11 (5): 260–287. https://doi.org/10.1007/BF02861195

  5. Anderson, L.E. (2000) Charles E. Allen and Sex Chromosomes. The Bryologist 103 (3): 442–448. https://doi.org/10.1639/0007-2745(2000)103[0442:CEAASC]2.0.CO;2

  6. Arnqvist, G. & Rowe, L. (2005) Sexual Conflict. Princeton University Press, 330 pp. https://doi.org/10.1515/9781400850600

  7. Avia, K., Lipinska, A.P., Mignerot, L., Montecinos, A.E., Jamy, M., Ahmed, S., Valero, M., Peters, A.F., Cock, J.M., Roze, D. & Coelho, S.M. (2018) Genetic Diversity in the UV Sex Chromosomes of the Brown Alga Ectocarpus. Genes 9 (6): 286. https://doi.org/10.3390/genes9060286

  8. Bachtrog, D., Kirkpatrick, M., Mank, J.E., McDaniel, S.F., Pires, J.C., Rice, W. & Valenzuela, N. (2011) Are all sex chromosomes created equal? Trends in genetics: TIG 27 (9): 350–357. https://doi.org/10.1016/j.tig.2011.05.005

  9. Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity 2 (Pt. 3): 349–368. https://doi.org/10.1038/hdy.1948.21

  10.  

  11. Baughman, J.T., Payton, A.C., Paasch, A.E., Fisher, K.M. & McDaniel, S.F. (2017) Multiple factors influence population sex ratios in the Mojave Desert moss Syntrichia caninervis. American journal of botany 104 (5): 733–742. https://doi.org/10.3732/ajb.1700045

  12. Bazzicalupo, A.L., Carpentier, F., Otto, S.P. & Giraud, T. (2019) Little Evidence of Antagonistic Selection in the Evolutionary Strata of Fungal Mating-Type Chromosomes (Microbotryum lychnidis-dioicae). G3 9 (6): 1987–1998. https://doi.org/10.1534/g3.119.400242

  13. Begun, D.J. & Aquadro, C.F. (1992) Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature 356 (6369): 519–520. https://doi.org/10.1038/356519a0

  14. Bengtsson, B.O. & Cronberg, N. (2009) The effective size of bryophyte populations. Journal of theoretical biology 258 (1): 121–126. https://doi.org/10.1016/j.jtbi.2009.01.002

  15. Berger, F. (2019) Emil Heitz, a true epigenetics pioneer. Nature reviews. Molecular cell biology 20 (10): 572. https://doi.org/10.1038/s41580-019-0161-z

  16. Bonduriansky, R., Maklakov, A., Zajitschek, F. & Brooks, R. (2008) Sexual Selection, Sexual Conflict and the Evolution of Ageing and Life Span. Functional ecology 22 (3): 443–453. https://doi.org/10.1111/j.1365-2435.2008.01417.x

  17. Bopp, M. (1957) Entwicklungsphysiologische Untersuchungen an Moosmutanten. Zeitschrift fur induktive Abstammungs-und Vererbungslehre 88 (4): 600–607. https://doi.org/10.1007/BF00309430

  18. Bowman, J.L., Kohchi, T., Yamato, K.T., Jenkins, J., Shu, S., Ishizaki, K., Yamaoka, S., Nishihama, R., Nakamura, Y., Berger, F., Adam, C., Aki, S.S., Althoff, F., Araki, T., Arteaga-Vazquez, M.A., Balasubrmanian, S., Barry, K., Bauer, D., Boehm, C.R., Briginshaw, L., Caballero-Perez, J., Catarino, B., Chen, F., Chiyoda, S., Chovatia, M., Davies, K.M., Delmans, M., Demura, T., Dierschke, T., Dolan, L., Dorantes-Acosta, A.E., Eklund, D.M., Florent, S.N., Flores-Sandoval, E., Fujiyama, A., Fukuzawa, H., Galik, B., Grimanelli, D., Grimwood, J., Grossniklaus, U., Hamada, T., Haseloff, J., Hetherington, A.J., Higo, A., Hirakawa, Y., Hundley, H.N., Ikeda, Y., Inoue, K., Inoue, S.-I., Ishida, S., Jia, Q., Kakita, M., Kanazawa, T., Kawai, Y., Kawashima, T., Kennedy, M., Kinose, K., Kinoshita, T., Kohara, Y., Koide, E., Komatsu, K., Kopischke, S., Kubo, M., Kyozuka, J., Lagercrantz, U., Lin, S.-S., Lindquist, E., Lipzen, A.M., Lu, C.-W., De Luna, E., Martienssen, R.A., Minamino, N., Mizutani, M., Mizutani, M., Mochizuki, N., Monte, I., Mosher, R., Nagasaki, H., Nakagami, H., Naramoto, S., Nishitani, K., Ohtani, M., Okamoto, T., Okumura, M., Phillips, J., Pollak, B., Reinders, A., Rövekamp, M., Sano, R., Sawa, S., Schmid, M.W., Shirakawa, M., Solano, R., Spunde, A., Suetsugu, N., Sugano, S., Sugiyama, A., Sun, R., Suzuki, Y., Takenaka, M., Takezawa, D., Tomogane, H., Tsuzuki, M., Ueda, T., Umeda, M., Ward, J.M., Watanabe, Y., Yazaki, K., Yokoyama, R., Yoshitake, Y., Yotsui, I., Zachgo, S. & Schmutz, J. (2017) Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. Cell 171 (2): 287–304. https://doi.org/10.1016/j.cell.2017.09.030

  19. Branco, S., Badouin, H., Rodríguez, de la Vega, R.C., Gouzy, J., Carpentier, F., Aguileta, G., Siguenza, S., Brandenburg, J.-T., Coelho, M.A., Hood, M.E. & Giraud, T. (2017) Evolutionary strata on young mating-type chromosomes despite the lack of sexual antagonism. Proceedings of the National Academy of Sciences of the United States of America 114 (27): 7067–7072. https://doi.org/10.1073/pnas.1701658114

  20. Bravo Núñez, M.A., Nuckolls, N.L. & Zanders, S.E. (2018) Genetic Villains: Killer Meiotic Drivers. Trends in genetics 34 (6): 424–433. https://doi.org/10.1016/j.tig.2018.02.003

  21. Budke, J.M. (2019) The moss calyptra: A maternal structure influencing offspring development. The Bryologist 122 (3): 471–491. https://doi.org/10.1639/0007-2745-122.3.471

  22. Bull, J.J. (1983) Evolution of sex determining mechanisms.The Benjamin/Cummings Publishing Company, Inc.

  23. Carey, S.B., Jenkins, J., Payton, A.C., Shu, S., Lovell, J.T., Maumus, F., Sreedasyam, A., Tiley, G.P., Fernandez-Pozo, N., Barry, K., Chen, C., Wang, M., Lipzen, A., Daum, C., Saski, C.A., McBreen, J.C., Conrad, R.E., Kollar, L.M., Olsson, S., Huttunen, S., Landis, J.B., Gordon Burleigh, J., Wickett, N.J., Johnson, M.G., Rensing, S.A., Grimwood, J., Schmutz, J. & McDaniel, S.F. (2020) Chromosome fusions shape an ancient UV sex chromosome system. bioRxiv. https://doi.org/10.1101/2020.07.03.163634

  24. Chapman, T. (2006) Evolutionary conflicts of interest between males and females. Current biology 16 (17): R744–54. https://doi.org/10.1016/j.cub.2006.08.020

  25. Charlesworth, B. & Charlesworth, D. (1978) A model for the evolution of dioecy and gynodioecy. The American naturalist 112. https://doi.org/10.1086/283342

  26. Charlesworth, B. (2009) Effective population size and patterns of molecular evolution and variation. Nature reviews. Genetics 10 (3): 195–205. https://doi.org/10.1038/nrg2526

  27. Charlesworth, B. & Charlesworth, D. (2000) The degeneration of Y chromosomes. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 355 (1403): 1563–1572. https://doi.org/10.1098/rstb.2000.0717

  28. Coelho, S.M., Gueno, J., Lipinska, A.P., Cock, J.M. & Umen, J.G. (2018) UV Chromosomes and Haploid Sexual Systems. Trends in plant science 23 (9): 794–807. https://doi.org/10.1016/j.tplants.2018.06.005

  29. Comeron, J.M., Williford, A. & Kliman, R.M. (2008) The Hill–Robertson effect: evolutionary consequences of weak selection and linkage in finite populations. Heredity 100 (1): 19–31. https://doi.org/10.1038/sj.hdy.6801059

  30. Crespi, B. & Nosil, P. (2013) Conflictual speciation: species formation via genomic conflict. Trends in ecology & evolution 28 (1): 48–57. https://doi.org/10.1016/j.tree.2012.08.015

  31. Cronberg, N., Natcheva, R. & Hedlund, K. (2006) Microarthropods mediate sperm transfer in mosses. Science 313 (5791): 1255. https://doi.org/10.1126/science.1128707

  32. De Clerck, O., Kao, S.-M., Bogaert, K.A., Blomme, J., Foflonker, F., Kwantes, M., Vancaester, E., Vanderstraeten, L., Aydogdu, E., Boesger, J., Califano, G., Charrier, B., Clewes, R., Del Cortona, A., D’Hondt, S., Fernandez-Pozo, N., Gachon, C.M., Hanikenne, M., Lattermann, L., Leliaert, F., Liu, X., Maggs, C.A., Popper, Z.A., Raven, J.A., Van Bel, M., Wilhelmsson, P.K.I., Bhattacharya, D., Coates, J.C., Rensing, S.A., Van Der Straeten, D., Vardi, A., Sterck, L., Vandepoele, K., Van de Peer, Y., Wichard, T. & Bothwell, J.H. (2018) Insights into the Evolution of Multicellularity from the Sea Lettuce Genome. Current biology 28 (18): 2921–2933. https://doi.org/10.1016/j.cub.2018.08.015

  33. Dufaÿ, M., Champelovier, P., Käfer, J., Henry, J.-P., Mousset, S. & Marais, G.A.B. (2014) An angiosperm-wide analysis of the gynodioecy--dioecy pathway. Annals of botany 114 (3): 539–548. https://doi.org/10.1093/aob/mcu134

  34. Ellegren, H. & Parsch, J. (2007) The evolution of sex-biased genes and sex-biased gene expression. Nature reviews. Genetics 8 (9): 689–698. https://doi.org/10.1038/nrg2167

  35. Eppley, S.M., Taylor, P.J. & Jesson, L.K. (2007) Self-fertilization in mosses: a comparison of heterozygote deficiency between species with combined versus separate sexes. Heredity 98 (1): 38–44. https://doi.org/10.1038/sj.hdy.6800900

  36. Ferris, P., Olson, B.J.S.C., De Hoff, P.L., Douglass, S., Casero, D., Prochnik, S., Geng, S., Rai, R., Grimwood, J., Schmutz, J., Nishii, I., Hamaji, T., Nozaki, H., Pellegrini, M. & Umen, J.G. (2010) Evolution of an expanded sex-determining locus in Volvox. Science 328 (5976): 351–354. https://doi.org/10.1126/science.1186222

  37. Furman, B.L.S., Metzger, D.C.H., Darolti, I., Wright, A.E., Sandkam, B.A., Almeida, P., Shu, J.J. & Mank, J.E. (2020) Sex Chromosome Evolution: So Many Exceptions to the Rules. Genome biology and evolution 12 (6): 750–763. https://doi.org/10.1093/gbe/evaa081

  38. Fuselier, L. (2008) Variation in life history characteristics between asexual and sexual populations of marchantia inflexa. The Bryologist 111 (2): 248–259. https://doi.org/10.1639/0007-2745(2008)111[248:VILHCB]2.0.CO;2

  39. Guillemin, M.-L., Huanel, O.R. & Martínez, E.A. (2012) Characterization of genetic markers linked to sex determination in the haploid‐diploid red alga gracilaria chilensis. Journal of phycology 48 (2): 365–372. https://doi.org/10.1111/j.1529-8817.2012.01116.x

  40. Haig, D. (2013) Filial mistletoes: the functional morphology of moss sporophytes. Annals of botany 111 (3): 337–345. https://doi.org/10.1093/aob/mcs295

  41. Haig, D. (2010) Games in tetrads: segregation, recombination, and meiotic drive. The American naturalist 176 (4): 404–413. https://doi.org/10.1086/656265

  42. Haig, D. & Wilczek, A. (2006) Sexual conflict and the alternation of haploid and diploid generations. Philosophical transactions of the Royal Society of London. Series B, Biological sciences 361 (1466): 335–343. https://doi.org/10.1098/rstb.2005.1794

  43. Hall, D.W. (2004) Meiotic drive and sex chromosome cycling. Evolution; international journal of organic evolution 58 (5): 925–931. https://doi.org/10.1111/j.0014-3820.2004.tb00426.x

  44. Hamaji, T., Mogi, Y., Ferris, P.J., Mori, T., Miyagishima, S., Kabeya, Y., Nishimura, Y., Toyoda, A., Noguchi, H., Fujiyama, A., Olson, B.J.S.C., Marriage, T.N., Nishii, I., Umen, J.G. & Nozaki, H. (2016) Sequence of the Gonium pectorale Mating Locus Reveals a Complex and Dynamic History of Changes in Volvocine Algal Mating Haplotypes. G3 6 (5): 1179–1189. https://doi.org/10.1534/g3.115.026229

  45. Hammond, T.M., Rehard, D.G., Xiao, H. & Shiu, P.K.T. (2012) Molecular dissection of Neurospora Spore killer meiotic drive elements. Proceedings of the National Academy of Sciences of the United States of America 109 (30): 12093–12098. https://doi.org/10.1073/pnas.1203267109

  46. Hedenäs, L. & Bisang, I. (2011) The overlooked dwarf males in mosses—Unique among green land plants. Perspectives in plant ecology, evolution and systematics 13 (2): 121–135. https://doi.org/10.1016/j.ppees.2011.03.001

  47. Heitz, E. (1928) Das heterochromatin der moose.Bornträger.

  48. Herron, M.D., Hackett, J.D., Aylward, F.O. & Michod, R.E. (2009) Triassic origin and early radiation of multicellular volvocine algae. Proceedings of the National Academy of Sciences of the United States of America 106 (9): 3254–3258. https://doi.org/10.1073/pnas.0811205106

  49. Hough, J., Wang, W., Barrett, S.C.H. & Wright, S.I. (2017) Hill-Robertson Interference Reduces Genetic Diversity on a Young Plant Y-Chromosome. Genetics 207 (2): 685–695. https://doi.org/10.1534/genetics.117.300142

  50. Immler, S. & Otto, S.P. (2015) The evolution of sex chromosomes in organisms with separate haploid sexes. Evolution; international journal of organic evolution 69 (3): 694–708. https://doi.org/10.1111/evo.12602

  51. Ironside, J.E. (2010) No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution. BioEssays: news and reviews in molecular, cellular and developmental biology 32 (8): 718–726. https://doi.org/10.1002/bies.200900124

  52. Korpelainen, H., Bisang, I., Hedenäs, L. & Kolehmainen, J. (2008) The first sex-specific molecular marker discovered in the moss Pseudocalliergon trifarium. The Journal of heredity 99 (6): 581–587. https://doi.org/10.1093/jhered/esn036

  53. Laenen, B., Machac, A., Gradstein, S.R., Shaw, B., Patiño, J., Désamoré, A., Goffinet, B., Cox, C.J., Shaw, A.J. & Vanderpoorten, A. (2016) Increased diversification rates follow shifts to bisexuality in liverworts. The New phytologist 210 (3): 1121–1129. https://doi.org/10.1111/nph.13835

  54. Lessells, C.M. & Parker, G.A. (1999) Parent—offspring conflict: the full–sib—half–sib fallacy. Proceedings of the Royal Society of London. Series B: Biological Sciences 266 (1429): 1637–1643. https://doi.org/10.1098/rspb.1999.0826

  55. Lipinska, A., Cormier, A., Luthringer, R., Peters, A.F., Corre, E., Gachon, C.M.M., Cock, J.M. & Coelho, S.M. (2015) Sexual dimorphism and the evolution of sex-biased gene expression in the brown alga ectocarpus. Molecular biology and evolution 32 (6): 1581–1597. https://doi.org/10.1093/molbev/msv049

  56. Lipinska, A.P., Toda, N.R.T., Heesch, S., Peters, A.F., Cock, J.M. & Coelho, S.M. (2017) Multiple gene movements into and out of haploid sex chromosomes. Genome biology 18 (1): 104. https://doi.org/10.1186/s13059-017-1201-7

  57. Luthringer, R., Cormier, A., Ahmed, S., Peters, A.F., Cock, J.M. & Coelho, S.M. (2014) Sexual dimorphism in the brown algae. Perspectives in Phycology 1 (1): 11–25. https://doi.org/10.1127/2198-011X/2014/0002

  58. Luthringer, R., Lipinska, A.P., Roze, D., Cormier, A., Macaisne, N., Peters, A.F., Cock, J.M. & Coelho, S.M. (2015) The Pseudoautosomal Regions of the U/V Sex Chromosomes of the Brown Alga Ectocarpus Exhibit Unusual Features. Molecular biology and evolution 32 (11): 2973–2985. https://doi.org/10.1093/molbev/msv173

  59. Lyttle, T.W. (1993) Cheaters sometimes prosper: distortion of mendelian segregation by meiotic drive. Trends in genetics 9 (6): 205–210. https://doi.org/10.1016/0168-9525(93)90120-7

  60. Mank, J.E. (2013) Sex chromosome dosage compensation: definitely not for everyone. Trends in genetics 29 (12): 677–683. https://doi.org/10.1016/j.tig.2013.07.005

  61. McDaniel, S.F. (2009) The Genetic Basis of Natural Variation in Bryophyte Model Systems, In: Roberts J.A. (Ed.) Annual Plant Reviews online, Vol. 46. John Wiley & Sons, Ltd. Chichester, UK, pp. 16–41. https://doi.org/10.1002/9781119312994.apr0385

  62. McDaniel, S.F., Atwood, J. & Burleigh, J.G. (2013) Recurrent evolution of dioecy in bryophytes. Evolution; international journal of organic evolution 67 (2): 567–572. https://doi.org/10.1111/j.1558-5646.2012.01808.x

  63.  

  64. McDaniel, S.F., Neubig, K.M., Payton, A.C., Quatrano, R.S. & Cove, D.J. (2013) Recent gene‐capture on the uv sex chromosomes of the moss ceratodon purpureus. Evolution 67 (10): 2811–2822. https://doi.org/10.1111/evo.12165

  65. McDaniel, S.F. & Perroud, P.-F. (2012) Invited perspective: bryophytes as models for understanding the evolution of sexual systems. The Bryologist 115 (1): 1–11. https://doi.org/10.1639/0007-2745-115.1.1

  66. McDaniel, S.F., Willis, J.H. & Shaw, A.J. (2007) A linkage map reveals a complex basis for segregation distortion in an interpopulation cross in the moss Ceratodon purpureus. Genetics 176 (4): 2489–2500. https://doi.org/10.1534/genetics.107.075424

  67. McLetchie, D.N. & Puterbaugh, M.N. (2000) Population sex ratios, sex-specific clonal traits and tradeoffs among these traits in the liverwort Marchantia inflexa. Oikos 90 (2): 227–237. https://doi.org/10.1034/j.1600-0706.2000.900203.x

  68. Montgomery, S.A., Tanizawa, Y., Galik, B., Wang, N., Ito, T., Mochizuki, T., Akimcheva, S., Bowman, J.L., Cognat, V., Maréchal-Drouard, L., Ekker, H., Hong, S.-F., Kohchi, T., Lin, S.-S., Liu, L.-Y.D., Nakamura, Y., Valeeva, L.R., Shakirov, E.V., Shippen, D.E., Wei, W.-L., Yagura, M., Yamaoka, S., Yamato, K.T., Liu, C. & Berger, F. (2020) Chromatin Organization in Early Land Plants Reveals an Ancestral Association between H3K27me3, Transposons, and Constitutive Heterochromatin. Current biology 30 (4): 573–588. https://doi.org/10.1016/j.cub.2019.12.015

  69. Muller, H.J. (1932) Some Genetic Aspects of Sex. The American naturalist 66 (703): 118–138. https://doi.org/10.1086/280418

  70. Müller, N.A., Kersten, B., Leite Montalvão, A.P., Mähler, N., Bernhardsson, C., Bräutigam, K., Carracedo Lorenzo, Z., Hoenicka, H., Kumar, V., Mader, M., Pakull, B., Robinson, K.M., Sabatti, M., Vettori, C., Ingvarsson, P.K., Cronk, Q., Street, N.R. & Fladung, M. (2020) A single gene underlies the dynamic evolution of poplar sex determination. Nature plants 6 (6): 630–637. https://doi.org/10.1038/s41477-020-0672-9

  71. Nauta, M.J. & Hoekstra, R.F. (1993) Evolutionary dynamics of spore killers. Genetics 135 (3): 923–930. https://doi.org/10.1093/genetics/135.3.923

  72. Norrell, T.E., Jones, K.S., Payton, A.C. & McDaniel, S.F. (2014) Meiotic sex ratio variation in natural populations of Ceratodon purpureus (Ditrichaceae). American journal of botany 101 (9): 1572–1576. https://doi.org/10.3732/ajb.1400156

  73. Okada, S., Sone, T., Fujisawa, M., Nakayama, S., Takenaka, M., Ishizaki, K., Kono, K., Shimizu-Ueda, Y., Hanajiri, T., Yamato, K.T., Fukuzawa, H., Brennicke, A. & Ohyama, K. (2001) The Y chromosome in the liverwort Marchantia polymorpha has accumulated unique repeat sequences harboring a male-specific gene. Proceedings of the National Academy of Sciences of the United States of America 98 (16): 9454–9459. https://doi.org/10.1073/pnas.171304798

  74. Otto, S.P., Pannell, J.R., Peichel, C.L., Ashman, T.-L., Charlesworth, D., Chippindale, A.K., Delph, L.F., Guerrero, R.F., Scarpino, S.V. & McAllister, B.F. (2011) About PAR: the distinct evolutionary dynamics of the pseudoautosomal region. Trends in genetics 27 (9): 358–367. https://doi.org/10.1016/j.tig.2011.05.001

  75. Parker, G.A. & Others (1979) Sexual selection and sexual conflict. Sexual selection and reproductive competition in insects 123: 166. https://doi.org/10.1016/B978-0-12-108750-0.50010-0

  76. Price, T.A.R., Hurst, G.D.D. & Wedell, N. (2010) Polyandry prevents extinction. Current biology 20 (5): 471–475. https://doi.org/10.1016/j.cub.2010.01.050

  77. Reik, W. & Walter, J. (2001) Genomic imprinting: parental influence on the genome. Nature reviews. Genetics 2 (1): 21–32. https://doi.org/10.1038/35047554

  78. Renner, S.S. (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American journal of botany 101 (10): 1588–1596. https://doi.org/10.3732/ajb.1400196

  79. Renner, S.S., Heinrichs, J. & Sousa, A. (2017) The sex chromosomes of bryophytes: Recent insights, open questions, and reinvestigations of Frullania dilatata and Plagiochila asplenioides. Journal of Systematics and Evolution 55 (4): 333–339. https://doi.org/10.1111/jse.12266

  80. Reski, R. (1998) Development, Genetics and Molecular Biology of Mosses. Botanica acta: Berichte der Deutschen Botanischen Gesellschaft = journal of the German Botanical Society 111 (1): 1–15. https://doi.org/10.1111/j.1438-8677.1998.tb00670.x

  81.  

  82.  

  83. Rice, W.R. (1987) The Accumulation of Sexually Antagonistic Genes as a Selective Agent Promoting the Evolution of Reduced Recombination between Primitive Sex Chromosomes. Evolution; international journal of organic evolution 41 (4): 911–914. https://doi.org/10.2307/2408899

  84. Robert, T. (1972) Parental investment and sexual selection. Sexual Selection & the Descent of Man, Aldine de Gruyter, New York:, pp. 136–179.

  85. Rosengren, F. & Cronberg, N. (2014) The adaptive background of nannandry: dwarf male distribution and fertilization in the moss Homalothecium lutescens. Biological journal of the Linnean Society. Linnean Society of London 113 (1): 74–84. https://doi.org/10.1111/bij.12332

  86. Rosenstiel, T.N., Shortlidge, E.E., Melnychenko, A.N., Pankow, J.F. & Eppley, S.M. (2012) Sex-specific volatile compounds influence microarthropod-mediated fertilization of moss. Nature 489 (7416): 431–433. https://doi.org/10.1038/nature11330

  87. Sayres, M.A.W. (2018) Genetic diversity on the sex chromosomes. Genome biology and evolution 10 (4): 1064. https://doi.org/10.1093/gbe/evy039

  88. Shaw, A.J. & Gaughan, J.F. (1993) Control of sex ratios in haploid populations of the moss, ceratodon purpureus. American journal of botany 80 (5): 584–591. https://doi.org/10.1002/j.1537-2197.1993.tb13844.x

  89. Shortlidge, E.E., Payton, A.C., Carey, S.B., McDaniel, S.F., Rosenstiel, T.N. & Eppley, S.M. (2020) Microarthropod contributions to fitness variation in the common moss Ceratodon purpureus. bioRxiv. [Online] https://doi.org/10.1101/2020.12.02.408872

  90. Stark, L.R., Brinda, J.C. & McLetchie, D.N. (2009) An experimental demonstration of the cost of sex and a potential resource limitation on reproduction in the moss Pterygoneurum (Pottiaceae). American journal of botany 96 (9): 1712–1721. https://doi.org/10.3732/ajb.0900084

  91. Szövényi, P., Perroud, P.-F., Symeonidi, A., Stevenson, S., Quatrano, R.S., Rensing, S.A., Cuming, A.C. & McDaniel, S.F. (2015) De novo assembly and comparative analysis of the Ceratodon purpureus transcriptome. Molecular ecology resources 15 (1): 203–215. https://doi.org/10.1111/1755-0998.12284

  92. Tao, Y., Araripe, L., Kingan, S.B., Ke, Y., Xiao, H. & Hartl, D.L. (2007) A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS biology 5 (11): e293. https://doi.org/10.1371/journal.pbio.0050293

  93. Tree of Sex Consortium (2014) Tree of Sex: A database of sexual systems. Scientific Data: 1. https://doi.org/10.1038/sdata.2014.15

  94. Vicoso, B. (2019) Molecular and evolutionary dynamics of animal sex-chromosome turnover. Nature ecology & evolution 3 (12): 1632–1641. https://doi.org/10.1038/s41559-019-1050-8

  95. Vicoso, B. & Charlesworth, B. (2006) Evolution on the X chromosome: unusual patterns and processes. Nature reviews. Genetics 7 (8): 645–653. https://doi.org/10.1038/nrg1914

  96. Villarreal, J.C. & Renner, S.S. (2013) Correlates of monoicy and dioicy in hornworts, the apparent sister group to vascular plants. BMC evolutionary biology 13: 239. https://doi.org/10.1186/1471-2148-13-239

  97. Voglmayr, H. (2000) Nuclear DNA Amounts in Mosses (Musci). Annals of botany 85 (4): 531–546. https://doi.org/10.1006/anbo.1999.1103

  98. Werren, J.H. (2011) Selfish genetic elements, genetic conflict, and evolutionary innovation. Proceedings of the National Academy of Sciences of the United States of America 108 Suppl 2: 10863–10870. https://doi.org/10.1073/pnas.1102343108

  99. Werren, J.H. & Beukeboom, L.W. (1998) Sex determination, sex ratios, and genetic conflict. Annual review of ecology and systematics 29 (1): 233–261. https://doi.org/10.1146/annurev.ecolsys.29.1.233

  100. Westergaard, M. (1958) The mechanism of sex determination in dioecious flowering plants. Advances in genetics 9: 217–281. https://doi.org/10.1016/S0065-2660(08)60163-7

  101. Yamato, K.T., Ishizaki, K., Fujisawa, M., Okada, S., Nakayama, S., Fujishita, M., Bando, H., Yodoya, K., Hayashi, K., Bando, T., Hasumi, A., Nishio, T., Sakata, R., Yamamoto, M., Yamaki, A., Kajikawa, M., Yamano, T., Nishide, T., Choi, S.-H., Shimizu-Ueda, Y., Hanajiri, T., Sakaida, M., Kono, K., Takenaka, M., Yamaoka, S., Kuriyama, C., Kohzu, Y., Nishida, H., Brennicke, A., Shin-i, T., Kohara, Y., Kohchi, T., Fukuzawa, H. & Ohyama, K. (2007) Gene organization of the liverwort Y chromosome reveals distinct sex chromosome evolution in a haploid system. Proceedings of the National Academy of Sciences 104 (15): 6472–6477. https://doi.org/10.1073/pnas.0609054104

  102. Yamazaki, T., Ichihara, K., Suzuki, R., Oshima, K., Miyamura, S., Kuwano, K., Toyoda, A., Suzuki, Y., Sugano, S., Hattori, M. & Kawano, S. (2017) Genomic structure and evolution of the mating type locus in the green seaweed Ulva partita. Scientific reports 7 (1): 11679. https://doi.org/10.1038/s41598-017-11677-0

  103. Zeh, D.W. & Zeh, J.A. (2000) Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays: news and reviews in molecular, cellular and developmental biology 22 (10): 938–946. https://doi.org/10.1002/1521-1878(200010)22:10<938::AID-BIES9>3.0.CO;2-9