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.
Downloads
References
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
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
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
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
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
Arnqvist, G. & Rowe, L. (2005) Sexual Conflict. Princeton University Press, 330 pp. https://doi.org/10.1515/9781400850600
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
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
Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity 2 (Pt. 3): 349–368. https://doi.org/10.1038/hdy.1948.21
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
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
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
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
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
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
Bopp, M. (1957) Entwicklungsphysiologische Untersuchungen an Moosmutanten. Zeitschrift fur induktive Abstammungs-und Vererbungslehre 88 (4): 600–607. https://doi.org/10.1007/BF00309430
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
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
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
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
Bull, J.J. (1983) Evolution of sex determining mechanisms.The Benjamin/Cummings Publishing Company, Inc.
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
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
Charlesworth, B. & Charlesworth, D. (1978) A model for the evolution of dioecy and gynodioecy. The American naturalist 112. https://doi.org/10.1086/283342
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
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
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
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
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
Cronberg, N., Natcheva, R. & Hedlund, K. (2006) Microarthropods mediate sperm transfer in mosses. Science 313 (5791): 1255. https://doi.org/10.1126/science.1128707
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
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
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
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
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
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
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
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
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
Haig, D. (2010) Games in tetrads: segregation, recombination, and meiotic drive. The American naturalist 176 (4): 404–413. https://doi.org/10.1086/656265
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
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
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
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
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
Heitz, E. (1928) Das heterochromatin der moose.Bornträger.
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Muller, H.J. (1932) Some Genetic Aspects of Sex. The American naturalist 66 (703): 118–138. https://doi.org/10.1086/280418
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
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
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
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
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
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
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
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
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
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
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
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
Robert, T. (1972) Parental investment and sexual selection. Sexual Selection & the Descent of Man, Aldine de Gruyter, New York:, pp. 136–179.
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
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
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
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
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
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
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
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
Tree of Sex Consortium (2014) Tree of Sex: A database of sexual systems. Scientific Data: 1. https://doi.org/10.1038/sdata.2014.15
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
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
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
Voglmayr, H. (2000) Nuclear DNA Amounts in Mosses (Musci). Annals of botany 85 (4): 531–546. https://doi.org/10.1006/anbo.1999.1103
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
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
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
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
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
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